Distinct behavioural and network correlates of two interneuron types in prefrontal cortex
Open accessAbstract
Neurons in the prefrontal cortex exhibit diverse behavioural correlates, an observation that has been attributed to cell-type diversity. To link identified neuron types with network and behavioural functions, we recorded from the two largest genetically defined inhibitory interneuron classes, the perisomatically targeting parvalbumin (PV) and the dendritically targeting somatostatin (SOM) neurons in anterior cingulate cortex of mice performing a reward foraging task. Here we show that PV and a subtype of SOM neurons form functionally homogeneous populations showing a double dissociation between both their inhibitory effects and behavioural correlates. Out of several events pertaining to behaviour, a subtype of SOM neurons selectively responded at reward approach, whereas PV neurons responded at reward leaving and encoded preceding stay duration. These behavioural correlates of PV and SOM neurons defined a behavioural epoch and a decision variable important for foraging (whether to stay or to leave), a crucial function attributed to the anterior cingulate cortex. Furthermore, PV neurons could fire in millisecond synchrony, exerting fast and powerful inhibition on principal cell firing, whereas the inhibitory effect of SOM neurons on firing output was weak and more variable, consistent with the idea that they respectively control the outputs of, and inputs to, principal neurons. These results suggest a connection between the circuit-level function of different interneuron types in regulating the flow of information and the behavioural functions served by the cortical circuits. Moreover, these observations bolster the hope that functional response diversity during behaviour can in part be explained by cell-type diversity.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In anterior cingulate cortex of mice performing a reward foraging task, a subgroup of narrow-spiking Sst interneurons fires preferentially at reward approach, while PV interneurons increase firing when the mouse leaves the reward location, correlated with stay duration in the reward zone.
“Extracellular recordings in the anterior cingulate cortex of mice performing a reward foraging task showed that a subgroup of optogenetically-identified Sst INs with narrow spikes fired preferentially at reward approach, whereas PV INs showed an increase firing when the mouse was leaving the reward location that was correlated with stay duration in the reward zone (Kvitsiani et al., 2013).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Kvitsiani et al., 2013
Split into 2 atoms — 1 confirmed, 0 partially supported, 1 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredPV+ interneurons exert fast and powerful inhibition on principal neuron firing, whereas SST+ interneurons exert weak and more variable inhibitory effects on firing output in behaving mice.
“PV+ interneurons, which could fire in millisecond synchrony, exert fast and powerful inhibition on principal neuron firing, whereas SST+ interneurons exert weak and more variable inhibitory effects on firing output in behaving mice 29.”
From Mechanisms of synaptic transmission dysregulation in the prefrontal cortex: pathophysiological implications (2022) · cites this paper as [29]
In mice performing a reward foraging task, SST+ interneurons in ACC selectively respond at reward approach, whereas PV+ interneurons respond at reward leaving.
“In mice performing a reward foraging task, SST+ interneurons in ACC are found to selectively respond at reward approach, whereas PV+ interneurons respond at reward leaving 29.”
From Mechanisms of synaptic transmission dysregulation in the prefrontal cortex: pathophysiological implications (2022) · cites this paper as [29]
These elements can be task-dependently recruited into larger brain networks for systems-level information processing and computation, representing their distal behavioural and cognitive functions.
“These elements can be task-dependently recruited into larger brain networks for systems-level information processing and computation, representing their distal behavioural and cognitive functions59,60.”
From The diversity of GABAergic neurons and neural communication elements (2019) · cites this paper as [59]
Local regions such as dACC can contain multiple, distinct neural population codes that encode distinct mental processes.
“This finding supports the idea that local regions such as dACC can contain multiple, distinct neural population codes25 that encode distinct mental processes.”
From Separate neural representations for physical pain and social rejection (2014) · cites this paper as [25]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Estimating the Number of Clusters in a Data Set Via the Gap Statistic
Tibshirani, R., Walther, G., & Hastie, T. (2001) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/1467-9868.00293 · Cited by 6,205 · see citing works
ASH, R. B. (1966) · Cited by 3,910 · see citing works
Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954 · see citing works
Parvalbumin neurons and gamma rhythms enhance cortical circuit performance
Sohal, V. S., Zhang, F., Yizhar, O., & Deisseroth, K. (2009) · Nature · doi:10.1038/nature07991 · Cited by 2,606 · see citing works
Driving fast-spiking cells induces gamma rhythm and controls sensory responses
Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H., & Moore, C. I. (2009) · Nature · doi:10.1038/nature08002 · Cited by 2,603 · see citing works
A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex
Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsani, D., Fu, Y., Lu, J., Lin, Y., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.026 · Cited by 1,828 · see citing works
Self-citationNeural correlations, population coding and computation
Averbeck, B. B., Latham, P. E., & Pouget, A. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1888 · Cited by 1,743 · see citing works
How Inhibition Shapes Cortical Activity
Isaacson, J. S., & Scanziani, M. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.027 · Cited by 1,678 · see citing works
Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex
The Petilla Interneuron Nomenclature Group (PING) (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2402 · Cited by 1,491 · see citing works
Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo
Klausberger, T., Magill, P. J., Márton, L. F., Roberts, J. D. B., Cobden, P. M., Buzsáki, G., & Somogyi, P. (2003) · Nature · doi:10.1038/nature01374 · Cited by 1,345 · see citing works
Neuron-type-specific signals for reward and punishment in the ventral tegmental area
Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B., & Uchida, N. (2012) · Nature · doi:10.1038/nature10754 · Cited by 1,318 · see citing works
A new metric for probability distributions
Endres, D., & Schindelin, J. E. (2003) · IEEE Transactions on Information Theory · doi:10.1109/tit.2003.813506 · Cited by 1,212 · see citing works
High-performance genetically targetable optical neural silencing by light-driven proton pumps
Chow, B. Y., Han, X., Dobry, A. S., Qian, X., Chuong, A. S., Li, M., Henninger, M. A., Belfort, G. M., Lin, Y., Monahan, P. E., et al. (2010) · Nature · doi:10.1038/nature08652 · Cited by 1,188 · see citing works
A Developmental Switch in the Response of DRG Neurons to ETS Transcription Factor Signaling
Hippenmeyer, S., Pecho‐Vrieseling, E., Sigrist, M., Portmann, T., Laengle, C., Ladle, D. R., & Arber, S. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030159 · Cited by 1,059 · see citing works
Barthó, P., Hirase, H., Monconduit, L., Zugaro, M. B., Harris, K. D., & Buzsáki, G. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01170.2003 · Cited by 888 · see citing works
Neural correlates, computation and behavioural impact of decision confidence
Kepecs, A., Uchida, N., Zariwala, H. A., & Mainen, Z. F. (2008) · Nature · doi:10.1038/nature07200 · Cited by 809 · see citing works
Disynaptic Inhibition between Neocortical Pyramidal Cells Mediated by Martinotti Cells
Silberberg, G., & Markram, H. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.012 · Cited by 768 · see citing works
Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition
Royer, S., Zemelman, B. V., Losonczy, A., Kim, J., Chance, F., Magee, J. C., & Buzsáki, G. (2012) · Nature Neuroscience · doi:10.1038/nn.3077 · Cited by 728 · see citing works
Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex
Fujisawa, S., Amarasingham, A., Harrison, M. T., & Buzsáki, G. (2008) · Nature Neuroscience · doi:10.1038/nn.2134 · Cited by 679 · see citing works
Quantitative measures of cluster quality for use in extracellular recordings
Schmitzer-Torbert, N. C., Jackson, J. C., Henze, D. A., Harris, K., & Redish, A. D. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.09.066 · Cited by 642 · see citing works
Kolling, N., Behrens, T. E. J., Mars, R. B., & Rushworth, M. F. S. (2012) · Science · doi:10.1126/science.1216930 · Cited by 629 · see citing works
Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli
Atallah, B. V., Bruns, W., Carandini, M., & Scanziani, M. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.013 · Cited by 612 · see citing works
Reliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus
Csicsvari, J., Hirase, H., Czurko, A., & Buzsáki, G. (1998) · Neuron · doi:10.1016/s0896-6273(00)80525-5 · Cited by 606 · see citing works
Mosaic Analysis with Double Markers in Mice
Zong, H., Espinosa, J. S., Su, H. H., Muzumdar, M. D., & Luo, L. (2005) · Cell · doi:10.1016/j.cell.2005.02.012 · Cited by 586 · see citing works
Neuronal basis of sequential foraging decisions in a patchy environment
Hayden, B. Y., Pearson, J. M., & Platt, M. L. (2011) · Nature Neuroscience · doi:10.1038/nn.2856 · Cited by 513 · see citing works
Millisecond-Timescale Optical Control of Neural Dynamics in the Nonhuman Primate Brain
Han, X., Qian, X., Bernstein, J. G., Zhou, H., Franzesi, G. T., Stern, P., Bronson, R. T., Graybiel, A. M., Desimone, R., & Boyden, E. S. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.011 · Cited by 497 · see citing works
Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex
Gentet, L. J., Kremer, Y., Taniguchi, H., Huang, Z. J., Staiger, J. F., & Petersen, C. C. H. (2012) · Nature Neuroscience · doi:10.1038/nn.3051 · Cited by 438 · see citing works
Self-citationDistinct Subtypes of Somatostatin-Containing Neocortical Interneurons Revealed in Transgenic Mice
Ma, Y., Hu, H., Berrebi, A. S., Mathers, P. H., & Agmon, A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0661-06.2006 · Cited by 432 · see citing works
Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex
Kapfer, C., Glickfeld, L. L., Atallah, B. V., & Scanziani, M. (2007) · Nature Neuroscience · doi:10.1038/nn1909 · Cited by 427 · see citing works
Regulation of neuronal input transformations by tunable dendritic inhibition
Lovett-Barron, M., Turi, G. F., Kaifosh, P., Lee, P. H., Bolze, F., Sun, X.-H., Nicoud, J.-F., Zemelman, B. V., Sternson, S. M., & Losonczy, A. (2012) · Nature Neuroscience · doi:10.1038/nn.3024 · Cited by 417 · see citing works
Temporal Interaction between Single Spikes and Complex Spike Bursts in Hippocampal Pyramidal Cells
Harris, K. D., Hirase, H., Leinekugel, X., Henze, D. A., & Buzsáki, G. (2001) · Neuron · doi:10.1016/s0896-6273(01)00447-0 · Cited by 388 · see citing works
Dendritic encoding of sensory stimuli controlled by deep cortical interneurons
Murayama, M., Pérez-Garci, E., Nevian, T., Bock, T., Senn, W., & Larkum, M. E. (2009) · Nature · doi:10.1038/nature07663 · Cited by 369 · see citing works
Lima, S. Q., Hromádka, T., Znamenskiy, P., & Zador, A. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006099 · Cited by 356 · see citing works
tFast Network Oscillations in the Hippocampal CA1 Region of the Behaving Rat
Csicsvari, T., Hirase, H., Czurkó, A., Mamiya, A., & Buzsáki, G. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-16-j0001.1999 · Cited by 353 · see citing works
A role for inhibition in shaping the temporal flow of information in prefrontal cortex
Constantinidis, C., Williams, G. V., & Goldman-Rakic, P. S. (2002) · Nature Neuroscience · doi:10.1038/nn799 · Cited by 348 · see citing works
Behavioral Shifts and Action Valuation in the Anterior Cingulate Cortex
Quilodran, R., Rothé, M., & Procyk, E. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.031 · Cited by 335 · see citing works
Correlations Without Synchrony
Brody, C. D. (1999) · Neural Computation · doi:10.1162/089976699300016133 · Cited by 329 · see citing works
Top-Down Control of Motor Cortex Ensembles by Dorsomedial Prefrontal Cortex
Narayanan, N. S., & Laubach, M. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.021 · Cited by 311 · see citing works
Functional, But Not Anatomical, Separation of “What” and “When” in Prefrontal Cortex
Machens, C. K., Romo, R., & Brody, C. D. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3276-09.2010 · Cited by 260 · see citing works
Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements
Isomura, Y., Harukuni, R., Takekawa, T., Aizawa, H., & Fukai, T. (2009) · Nature Neuroscience · doi:10.1038/nn.2431 · Cited by 230 · see citing works
Laminar specificity of functional input to distinct types of inhibitory cortical neurons
Xu, X., & Callaway, E. M. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4104-08.2009 · Cited by 218 · see citing works
Werd, H. J. J. M. V. D., Rajkowska, G., Evers, P., & Uylings, H. B. M. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0247-z · Cited by 191 · see citing works
Heterogeneous reward signals in prefrontal cortex
Wallis, J. D., & Kennerley, S. W. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.02.009 · Cited by 186 · see citing works
McGarry, L. M. (2010) · Frontiers in Neural Circuits · doi:10.3389/fncir.2010.00012 · Cited by 166 · see citing works
Marshall, L., Henze, D. A., Hirase, H., Leinekugel, X., Dragoi, G., & Buzsáki, G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-02-j0001.2002 · Cited by 119 · see citing works
Scaled correlation analysis: a better way to compute a cross‐correlogram
Nikolić, D., Muresan, R. C., Feng, W., & Singer, W. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07987.x · Cited by 111 · see citing works
Hartwich, K., Pollak, T., & Klausberger, T. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1397-09.2009 · Cited by 69 · see citing works
Complementary spatial firing in place cell-interneuron pairs
Hangya, B., Li, Y., Muller, R. U., & Czurkó, A. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.194274 · Cited by 45 · see citing works
Self-citation
Flagged first, then by citations
1 of the 49 references couldn’t be matched to a known paper.
Research works printed but not linked: 3
- [31]Sohal VS Zhang F Yizhar O Deisseroth K Parvalbumin neurons and gamma rhythms enhance cortical circuit performance Nature 459 698 702 2009 19396159 PMC3969859
- [37]Lima SQ Hromadka T Znamenskiy P Zador AM PINP: a new method of tagging neuronal populations for identification during in vivo electrophysiological recording PLoS One 4 e6099 2009 19584920 PMC2702752
- [46]Fujisawa S Amarasingham A Harrison MT Buzsaki G Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex Nat Neurosci 11 823 833 2008 18516033 PMC2562676
Cited by
Sorted by citations
GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits
Tremblay, R., Lee, S., & Rudy, B. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.033 · Cited by 2,033 · see citing works
“Extracellular recordings in the anterior cingulate cortex of mice performing a reward-foraging task showed that a subgroup of optogenetically identified Sst INs with narrow spikes fired preferentially at reward approach, whereas PV INs showed increased firing when the mouse was leaving the reward location that was cor…”
Hu, H., Gan, J., & Jonas, P. (2014) · Science · doi:10.1126/science.1255263 · Cited by 1,197 · see citing works
Optogenetics: 10 years of microbial opsins in neuroscience
Deisseroth, K. A. (2015) · Nature Neuroscience · doi:10.1038/nn.4091 · Cited by 1,286 · see citing works
Cortical interneurons that specialize in disinhibitory control
Pi, H.-J., Hangya, B., Kvitsiani, D., Sanders, J. I., Huang, Z. J., & Kepecs, A. (2013) · Nature · doi:10.1038/nature12676 · Cited by 1,136 · see citing works
Self-citationInterneuron cell types are fit to function
Kepecs, A., & Fishell, G. (2014) · Nature · doi:10.1038/nature12983 · Cited by 1,110 · see citing works
Building better biomarkers: brain models in translational neuroimaging
Woo, C.-W., Chang, L. J., Lindquist, M. A., & Wager, T. D. (2017) · Nature Neuroscience · doi:10.1038/nn.4478 · Cited by 1,056 · see citing works
Ventromedial hypothalamic neurons control a defensive emotion state
Kunwar, P. S., Zelikowsky, M., Remedios, R., Cai, H., Balban, M. Y., Meister, M., & Anderson, D. J. (2015) · eLife · doi:10.7554/elife.06633 · Cited by 1,112 · see citing works
Network abnormalities and interneuron dysfunction in Alzheimer disease
Palop, J. J., & Mucke, L. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.141 · Cited by 1,022 · see citing works
Dissociable dopamine dynamics for learning and motivation
Mohebi, A., Pettibone, J. R., Hamid, A., Wong, J.-M. T., Vinson, L. T., Patriarchi, T., Tian, L., Kennedy, R. T., & Berke, J. D. (2019) · Nature · doi:10.1038/s41586-019-1235-y · Cited by 714 · see citing works
Ferguson, B. R., & Gao, W.-J. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00037 · Cited by 594 · see citing works
Amygdala interneuron subtypes control fear learning through disinhibition
Wolff, S. B. E., Gründemann, J., Tovote, P., Krabbe, S., Jacobson, G. A., Müller, C. R., Herry, C., Ehrlich, I., Friedrich, R. W., Letzkus, J. J., et al. (2014) · Nature · doi:10.1038/nature13258 · Cited by 489 · see citing works
Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus
Lee, H., Kim, D.-W., Remedios, R., Anthony, T. E., Chang, A., Madisen, L., Zeng, H., & Anderson, D. J. (2014) · Nature · doi:10.1038/nature13169 · Cited by 479 · see citing works
Optogenetics for light control of biological systems
Emiliani, V., Entcheva, E. G., Hedrich, R., Hegemann, P., Konrad, K. R., Lüscher, C., Mahn, M., Pan, Z., Sims, R. R., Vierock, J., et al. (2022) · Nature Reviews Methods Primers · doi:10.1038/s43586-022-00136-4 · Cited by 482 · see citing works
Prefrontal Parvalbumin Neurons in Control of Attention
Kim, H., Ährlund‐Richter, S., Wang, X., Deisseroth, K. A., & Carlén, M. (2016) · Cell · doi:10.1016/j.cell.2015.11.038 · Cited by 456 · see citing works
Serotonin neurons in the dorsal raphe nucleus encode reward signals
Li, Y., Zhong, W., Wang, D., Feng, Q., Liu, Z., Zhou, J., Jia, C., Hu, F., Zeng, J., Guo, Q., et al. (2016) · Nature Communications · doi:10.1038/ncomms10503 · Cited by 420 · see citing works
Somatostatin-expressing neurons in cortical networks
Urban-Ciecko, J., & Barth, A. L. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.53 · Cited by 374 · see citing works
Arithmetic and local circuitry underlying dopamine prediction errors
Eshel, N., Bukwich, M., Rao, V., Hemmelder, V., Tian, J., & Uchida, N. (2015) · Nature · doi:10.1038/nature14855 · Cited by 386 · see citing works
Cell-Type-Specific Activity in Prefrontal Cortex during Goal-Directed Behavior
Pinto, L., & Dan, Y. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.021 · Cited by 323 · see citing works
Global Representations of Goal-Directed Behavior in Distinct Cell Types of Mouse Neocortex
Allen, W. E., Kauvar, I., Chen, M. Z., Richman, E. B., Yang, S., Chan, K. Y., Gradinaru, V., Deverman, B. E., Luo, L., & Deisseroth, K. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.017 · Cited by 369 · see citing works
Distinct inhibitory circuits orchestrate cortical beta and gamma band oscillations
Chen, G., Zhang, Y., Li, X., Zhao, X., Ye, Q., Lin, Y., Tao, H. W., Rasch, M. J., & Zhang, X. (2017) · Neuron · doi:10.1016/j.neuron.2017.11.033 · Cited by 345 · see citing works
Medial prefrontal cortex in neurological diseases
Xu, P., Chen, A., Li, Y., Xing, X., & Lü, H. (2019) · Physiological Genomics · doi:10.1152/physiolgenomics.00006.2019 · Cited by 346 · see citing works
Probing perceptual decisions in rodents
Carandini, M., & Churchland, A. K. (2013) · Nature Neuroscience · doi:10.1038/nn.3410 · Cited by 323 · see citing works
Tools for Probing Local Circuits: High-Density Silicon Probes Combined with Optogenetics
Buzsáki, G., Stark, E., Berényi, A., Khodagholy, D., Kipke, D. R., Yoon, E., & Wise, K. D. (2015) · Neuron · doi:10.1016/j.neuron.2015.01.028 · Cited by 328 · see citing works
Dopamine neurons share common response function for reward prediction error
Eshel, N., Tian, J., Bukwich, M., & Uchida, N. (2016) · Nature Neuroscience · doi:10.1038/nn.4239 · Cited by 306 · see citing works
Yan, Z., & Rein, B. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01092-3 · Cited by 300 · see citing works
“PV + interneurons, which could fi re in millisecond synchrony, exert fast and powerful inhibition on principal neuron fi ring, whereas SST + inter-neurons exert weak and more variable inhibitory effects on fi ring output in behaving mice [29].”
BackgroundSeparate neural representations for physical pain and social rejection
Woo, C.-W., Koban, L., Kross, E., Lindquist, M. A., Banich, M. T., Ruzic, L., Andrews-Hanna, J. R., & Wager, T. D. (2014) · Nature Communications · doi:10.1038/ncomms6380 · Cited by 310 · see citing works
A Unified Framework for Dopamine Signals across Timescales
Kim, H. R., Malik, A. N., Mikhael, J. G., Bech, P., Tsutsui‐Kimura, I., Sun, F., Zhang, Y., Li, Y., Watabe‐Uchida, M., Gershman, S. J., et al. (2020) · Cell · doi:10.1016/j.cell.2020.11.013 · Cited by 297 · see citing works
Large-Scale Meta-Analysis of Human Medial Frontal Cortex Reveals Tripartite Functional Organization
de la Vega, A. I., Chang, L. J., Banich, M. T., Wager, T. D., & Yarkoni, T. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4402-15.2016 · Cited by 288 · see citing works
A large fraction of neocortical myelin ensheathes axons of local inhibitory neurons
Micheva, K. D., Wolman, D. N., Mensh, B. D., Pax, E., Buchanan, J., Smith, S. J., & Bock, D. D. (2016) · eLife · doi:10.7554/elife.15784 · Cited by 271 · see citing works
Nakajima, M., Görlich, A., & Heintz, N. (2014) · Cell · doi:10.1016/j.cell.2014.09.020 · Cited by 262 · see citing works
Kragel, P. A., Kano, M., Van Oudenhove, L., Ly, H. G., Dupont, P., Rubio, A., Delon-Martin, C., Bonaz, B. L., Manuck, S. B., Gianaros, P. J., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0051-7 · Cited by 272 · see citing works
Microglia modulate blood flow, neurovascular coupling, and hypoperfusion via purinergic actions
Császár, E., Lénárt, N., Cserép, C., Környei, Z., Fekete, R., Pósfai, B., Balázsfi, D., Hangya, B., Schwarcz, A. D., Szabadits, E., et al. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20211071 · Cited by 263 · see citing works
Self-citationHu, H. (2016) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070815-014106 · Cited by 253 · see citing works
Prefrontal cortical control of a brainstem social behavior circuit
Franklin, T. B., Silva, B. A., Perova, Z., Marrone, L., Masferrer, M. E., Zhan, Y., Kaplan, A., Greetham, L., Verrechia, V., Halman, A., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4470 · Cited by 231 · see citing works
Dopamine reward prediction errors reflect hidden-state inference across time
Starkweather, C. K., Babayan, B. M., Uchida, N., & Gershman, S. J. (2017) · Nature Neuroscience · doi:10.1038/nn.4520 · Cited by 206 · see citing works
The diversity of GABAergic neurons and neural communication elements
Huang, Z. J., & Paul, A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0195-4 · Cited by 201 · see citing works
Neurodevelopment, GABA System Dysfunction, and Schizophrenia
Schmidt, M. J., & Mirnics, K. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.95 · Cited by 239 · see citing works
The role of population structure in computations through neural dynamics
Dubreuil, A., Valente, A., Beiran, M., Mastrogiuseppe, F., & Ostojic, S. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01088-4 · Cited by 237 · see citing works
Delay activity of specific prefrontal interneuron subtypes modulates memory-guided behavior
Kamigaki, T., & Dan, Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4554 · Cited by 208 · see citing works
McKlveen, J. M., Morano, R. L., Fitzgerald, M., Zoubovsky, S., Cassella, S. N., Scheimann, J. R., Ghosal, S., Mahbod, P., Packard, B. A., Myers, B., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.03.2101 · Cited by 224 · see citing works
Tasks for inhibitory interneurons in intact brain circuits
Roux, L., & Buzsáki, G. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.09.011 · Cited by 218 · see citing works
Distinct Roles of Parvalbumin- and Somatostatin-Expressing Interneurons in Working Memory
Kim, D., Jeong, H., Lee, J., Ghim, J.-W., Her, E. S., Lee, S.-H., & Jung, M. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.023 · Cited by 201 · see citing works
Distributed and Mixed Information in Monosynaptic Inputs to Dopamine Neurons
Tian, J., Huang, R., Cohen, J. Y., Osakada, F., Kobak, D., Machens, C. K., Callaway, E. M., Uchida, N., & Watabe-Uchida, M. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.018 · Cited by 224 · see citing works
Differential roles of medial prefrontal subregions in the regulation of drug seeking
Moorman, D. E., James, M. H., McGlinchey, E. M., & Aston‐Jones, G. (2014) · Brain Research · doi:10.1016/j.brainres.2014.12.024 · Cited by 224 · see citing works
Frontal cortex neuron types categorically encode single decision variables
Hirokawa, J., Vaughan, A., Masset, P., Ott, T., & Kepecs, Á. (2019) · Nature · doi:10.1038/s41586-019-1816-9 · Cited by 215 · see citing works
Prefrontal neuronal assemblies temporally control fear behaviour
Déjean, C., Courtin, J., Karalis, N., Chaudun, F., Wurtz, H., Bienvenu, T., & Herry, C. (2016) · Nature · doi:10.1038/nature18630 · Cited by 216 · see citing works
A distinct entorhinal cortex to hippocampal CA1 direct circuit for olfactory associative learning
Li, Y., Xu, J., Liu, Y., Zhu, J., Liu, N., Zeng, W., Huang, N., Rasch, M. J., Jiang, H., Gu, X., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4517 · Cited by 210 · see citing works
Regulation of REM and Non-REM Sleep by Periaqueductal GABAergic Neurons
Weber, F., Do, J. P. H., Chung, S., Beier, K. T., Bikov, M., Doost, M. S., & Dan, Y. (2018) · Nature Communications · doi:10.1038/s41467-017-02765-w · Cited by 214 · see citing works
Khan, A. G., Poort, J., Chadwick, A., Blot, A., Sahani, M., Mrsic‐Flogel, T. D., & Hofer, S. B. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0143-z · Cited by 205 · see citing works
Prefrontal somatostatin interneurons encode fear memory
Cummings, K. A., & Clem, R. L. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0552-7 · Cited by 209 · see citing works
Optogenetic dissection of medial prefrontal cortex circuitry
Riga, D., Matos, M. R., Glas, A., Smit, A. B., Spijker, S., & Van den Oever, M. C. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00230 · Cited by 208 · see citing works
Wang, G., Cen, C., Li, C. V., Cao, S., Wang, N., Zhou, Z., Liu, X., Xu, Y., Tian, N.-X., Zhang, Y., et al. (2015) · Nature Communications · doi:10.1038/ncomms8660 · Cited by 208 · see citing works
Serotonin, Amygdala and Fear: Assembling the Puzzle
Bocchio, M., McHugh, S. B., Bannerman, D. M., Sharp, T., & Capogna, M. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00024 · Cited by 207 · see citing works
The mouse prefrontal cortex: Unity in diversity
Le Merre, P., Ährlund-Richter, S., & Carlén, M. (2021) · Neuron · doi:10.1016/j.neuron.2021.03.035 · Cited by 207 · see citing works
Interneuron Types as Attractors and Controllers
Fishell, G., & Kepecs, Á. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050421 · Cited by 197 · see citing works
Complementary control of sensory adaptation by two types of cortical interneurons
Natan, R. G., Briguglio, J. J., Mwilambwe-Tshilobo, L., Jones, S. I., Aizenberg, M., Goldberg, E. M., & Geffen, M. N. (2015) · eLife · doi:10.7554/elife.09868 · Cited by 189 · see citing works
Decision Making: The Neuroethological Turn
Pearson, J. M., Watson, K. K., & Platt, M. L. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.037 · Cited by 184 · see citing works
Reconfigurable nanophotonic silicon probes for sub-millisecond deep-brain optical stimulation
Mohanty, A., Li, Q., Tadayon, M. A., Roberts, S. P., Bhatt, G. R., Shim, E., Ji, X., Cardenas, J., Miller, S. A., Kepecs, A., et al. (2020) · Nature Biomedical Engineering · doi:10.1038/s41551-020-0516-y · Cited by 188 · see citing works
Self-citationRecruitment of GABAergic Interneurons in the Barrel Cortex during Active Tactile Behavior
Yu, J., Hu, H., Agmon, A., & Svoboda, K. (2019) · Neuron · doi:10.1016/j.neuron.2019.07.027 · Cited by 186 · see citing works
Somatostatin-Expressing Inhibitory Interneurons in Cortical Circuits
Yavorska, I., & Wehr, M. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00076 · Cited by 185 · see citing works
Inhibitory Gating of Basolateral Amygdala Inputs to the Prefrontal Cortex
McGarry, L. M., & Carter, A. G. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.0874-16.2016 · Cited by 169 · see citing works
Abbas, A. I., Sundiang, M. J. M., Henoch, B., Morton, M. P., Bolkan, S. S., Park, A. J., Harris, A. Z., Kellendonk, C., & Gordon, J. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.029 · Cited by 183 · see citing works
Neuronal circuits in barrel cortex for whisker sensory perception
Staiger, J. F., & Petersen, C. C. H. (2021) · Physiological Reviews · doi:10.1152/physrev.00019.2019 · Cited by 165 · see citing works
A Disinhibitory Microcircuit Mediates Conditioned Social Fear in the Prefrontal Cortex
Xu, H., Liu, L., Tian, Y., Wang, J., Li, J., Zheng, J., Zhao, H., He, M., Xu, T.-L., Duan, S., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.026 · Cited by 181 · see citing works
Sun, Q., Li, X., Ren, M., Zhao, M., Zhong, Q., Ren, Y., Luo, P., Ni, H., Zhang, X., Zhang, C., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0429-9 · Cited by 175 · see citing works
Wager, T. D., Atlas, L. Y., Botvinick, M. M., Chang, L. J., Coghill, R. C., Davis, K. D., Iannetti, G. D., Poldrack, R. A., Shackman, A. J., & Yarkoni, T. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1600282113 · Cited by 162 · see citing works
Habenula Lesions Reveal that Multiple Mechanisms Underlie Dopamine Prediction Errors
Tian, J., & Uchida, N. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.028 · Cited by 165 · see citing works
A transcriptomic axis predicts state modulation of cortical interneurons
Bugeon, S., Duffield, J. A. M., Dipoppa, M., Ritoux, A., Prankerd, I., Nicoloutsopoulos, D., Orme, D., Shinn, M., Peng, H., Forrest, H., et al. (2022) · Nature · doi:10.1038/s41586-022-04915-7 · Cited by 177 · see citing works
Distinct and Dynamic ON and OFF Neural Ensembles in the Prefrontal Cortex Code Social Exploration
Liang, B., Zhang, L., Barbera, G., Fang, W., Zhang, J., Chen, X., Chen, R., Li, Y., & Lin, D. (2018) · Neuron · doi:10.1016/j.neuron.2018.08.043 · Cited by 170 · see citing works
Structured dendritic inhibition supports branch-selective integration in CA1 pyramidal cells
Bloss, E. B., Cembrowski, M. S., Karsh, B., Colonell, J., Fetter, R. D., & Spruston, N. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.029 · Cited by 164 · see citing works
Ito, A., Ure, K., Chen, H., Swann, J. W., & Zoghbi, H. Y. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.029 · Cited by 152 · see citing works
Orsini, C. A., Moorman, D. E., Young, J. W., Setlow, B., & Floresco, S. B. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.009 · Cited by 153 · see citing works
A dendritic disinhibitory circuit mechanism for pathway-specific gating
Yang, G. R., Murray, J. D., & Wang, X.-J. (2016) · Nature Communications · doi:10.1038/ncomms12815 · Cited by 148 · see citing works
Song, Y.-H., Yoon, J., & Lee, S. (2021) · Experimental & Molecular Medicine · doi:10.1038/s12276-021-00580-4 · Cited by 147 · see citing works
Dopamine facilitates associative memory encoding in the entorhinal cortex
Lee, J. Y., Jun, H., Soma, S., Nakazono, T., Shiraiwa, K., Dasgupta, A., Nakagawa, T., Xie, J. L., Chavez, J., Romo, R., et al. (2021) · Nature · doi:10.1038/s41586-021-03948-8 · Cited by 144 · see citing works
Genetic strategies to access activated neurons
DeNardo, L. A., & Luo, L. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.05.014 · Cited by 139 · see citing works
Functions and dysfunctions of neocortical inhibitory neuron subtypes
Hattori, R., Kuchibhotla, K. V., Froemke, R. C., & Komiyama, T. (2017) · Nature Neuroscience · doi:10.1038/nn.4619 · Cited by 142 · see citing works
Complementary networks of cortical somatostatin interneurons enforce layer specific control
Naka, A., Veit, J., Shababo, B., Chance, R. K., Risso, D., Stafford, D., Snyder, B., Egladyous, A., Chu, D., Sridharan, S., et al. (2019) · eLife · doi:10.7554/elife.43696 · Cited by 117 · see citing works
Miyoshi, G., Young, A., Petros, T., Karayannis, T., McKenzie Chang, M., Lavado, A., Iwano, T., Nakajima, M., Taniguchi, H., Huang, Z. J., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1164-15.2015 · Cited by 135 · see citing works
Self-citationFunctional fission of parvalbumin interneuron classes during fast network events
Varga, C., Oijala, M., Lish, J., Szabo, G. G., Bezaire, M., Marchionni, I., Golshani, P., & Soltesz, I. (2014) · eLife · doi:10.7554/elife.04006 · Cited by 130 · see citing works
Hamada, M., Galea, J. M., Lazzaro, V. D., Mazzone, P., Ziemann, U., & Rothwell, J. C. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1960-14.2014 · Cited by 137 · see citing works
Inhibitory stabilization and visual coding in cortical circuits with multiple interneuron subtypes
Litwin-Kumar, A., Rosenbaum, R., & Doiron, B. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00732.2015 · Cited by 138 · see citing works
Cholinergic modulation of spatial learning, memory and navigation
Solari, N., & Hangya, B. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14089 · Cited by 139 · see citing works
Self-citationLearning shapes the aversion and reward responses of lateral habenula neurons
Wang, D., Li, Y., Feng, Q., Guo, Q., Zhou, J., & Luo, M. (2017) · eLife · doi:10.7554/elife.23045 · Cited by 141 · see citing works
The medial prefrontal cortex shapes dopamine reward prediction errors under state uncertainty
Starkweather, C. K., Gershman, S. J., & Uchida, N. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.036 · Cited by 136 · see citing works
Spatiotemporal dynamics of noradrenaline during learned behaviour
Breton‐Provencher, V., Drummond, G. T., Feng, J., Li, Y., & Sur, M. (2022) · Nature · doi:10.1038/s41586-022-04782-2 · Cited by 135 · see citing works
Hu, H., Cavendish, J. Z., & Agmon, A. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00195 · Cited by 120 · see citing works
Rodgers, C. C., & DeWeese, M. R. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.031 · Cited by 130 · see citing works
dmPFC-vlPAG projection neurons contribute to pain threshold maintenance and antianxiety behaviors
Yin, J.-B., Liang, S., Li, F., Zhao, W., Bai, Y., Sun, Y., Wu, Z.-Y., Ding, T., Sun, Y., Liu, H., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci127607 · Cited by 134 · see citing works
Self-citationNeocortical Somatostatin Neurons Reversibly Silence Excitatory Transmission via GABAb Receptors
Urban‐Ciećko, J., Fanselow, E. E., & Barth, A. L. (2015) · Current Biology · doi:10.1016/j.cub.2015.01.035 · Cited by 126 · see citing works
Nonhuman Primate Optogenetics: Recent Advances and Future Directions
Galván, A., Stauffer, W. R., Acker, L., El-Shamayleh, Y., Inoue, K., Ohayon, S., & Schmid, M. C. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1839-17.2017 · Cited by 127 · see citing works
Asymmetric effects of activating and inactivating cortical interneurons
Phillips, E. A. K., & Hasenstaub, A. R. (2016) · eLife · doi:10.7554/elife.18383 · Cited by 127 · see citing works
Cortical Interneurons Differentially Shape Frequency Tuning following Adaptation
Natan, R. G., Rao, W., & Geffen, M. N. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.012 · Cited by 125 · see citing works
Stress-sensitive neural circuits change the gut microbiome via duodenal glands
Chang, H., Perkins, M. H., Novaes, L. S., Qian, F., Zhang, T., Neckel, P. H., Scherer, S., Ley, R. E., Han, W., & de Araújo, I. E. (2024) · Cell · doi:10.1016/j.cell.2024.07.019 · Cited by 133 · see citing works
Jia, X., Siegle, J. H., Bennett, C., Gale, S. D., Denman, D. J., Koch, C., & Olsen, S. R. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00680.2018 · Cited by 125 · see citing works
Sparta, D. R., Hovelsø, N., Mason, A. O., Kantak, P. A., Ung, R. L., Decot, H., & Stuber, G. D. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0235-13.2014 · Cited by 123 · see citing works
Task-dependent representations of stimulus and choice in mouse parietal cortex
Pho, G. N., Goard, M. J., Woodson, J., Crawford, B., & Sur, M. (2018) · Nature Communications · doi:10.1038/s41467-018-05012-y · Cited by 123 · see citing works
Anterior Cingulate Cortex and the Control of Dynamic Behavior in Primates
Monosov, I. E., Haber, S. N., Leuthardt, E. C., & Jezzini, A. (2020) · Current Biology · doi:10.1016/j.cub.2020.10.009 · Cited by 118 · see citing works
Top‐down and bottom‐up control of stress‐coping
de Kloet, E. R., de Kloet, S. F., de Kloet, C. S., & de Kloet, A. D. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12675 · Cited by 120 · see citing works
Dynamics of a disinhibitory prefrontal microcircuit in controlling social competition
Zhang, C., Zhu, H. L., Ni, Z., Xin, Q., Zhou, T., Wu, R., Gao, G., Gao, Z., Ma, H., Li, H., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.10.034 · Cited by 123 · see citing works
- Authors
- Kvitsiani, D., Ranade, S., Hangya, B., Taniguchi, H., Huang, J. Z., & Kepecs, A.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- Venue
- Nature
- Published
- 2013-05-26
- Volume
- 498
- Issue
- 7454
- Pages
- 363-366
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4349584
- OpenAlex
- W2012509205
- Cited by
- 516
- References
- 49
- Citations by year
- 2026: 20 · 2025: 49 · 2024: 45 · 2023: 39 · 2022: 36 · 2021: 36 · 2020: 43 · 2019: 48 · 2018: 34 · 2017: 39 · 2016: 41 · 2015: 35 · 2014: 37 · 2013: 14
- FWCI
- 23.13
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS075531)
- 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
- parvalbumin interneurons, somatostatin interneurons, inhibitory interneurons, anterior cingulate cortex, prefrontal cortex, neuronal synchronization, decision variables, stay duration, cortical circuits
- MeSH terms
- Animals, Feeding Behavior, Interneurons, Male, Neural Pathways, Parvalbumins, Reward, Somatostatin, Prefrontal Cortex, Mice, Single-Cell Analysis, Optogenetics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
