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Imaging Spatiotemporal Dynamics of Surround Inhibition in the Barrels Somatosensory Cortex
Open accessAbstract
Sensory processing and its perception require that local information would also be available globally. Indeed, in the mammalian neocortex, local excitation spreads over large distances via the long-range horizontal connections in layer 2/3 and may spread over an entire cortical area if excitatory polysynaptic pathways are also activated. Therefore, a balance between local excitation and surround inhibition is required. Here we explore the spatiotemporal aspects of cortical depolarization and hyperpolarization of rats anesthetized with urethane. New voltage-sensitive dyes (VSDs) were used for high-resolution real-time visualization of the cortical responses to whisker deflections and cutaneous stimulations of the whisker pad. These advances facilitated imaging of ongoing activity and evoked responses even without signal averaging. We found that the motion of a single whisker evoked a cortical response exhibiting either one or three phases. During a triphasic response, there was first a cortical depolarization in a small cortical region the size of a single cortical barrel. Subsequently, this depolarization increased and spread laterally in an oval manner, preferentially along rows of the barrel field. During the second phase, the amplitude of the evoked response declined rapidly, presumably because of recurrent inhibition. Subsequently, the third phase exhibiting a depolarization rebound was observed and clear, and approximately 16 Hz oscillations were detected. Stimulus conditions revealing a net surround hyperpolarization during the second phase were also found. By using new, improved VSD, the present findings shed new light on the spatial parameters of the intricate spatiotemporal cortical interplay of inhibition and excitation.
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“However, similar characteristic modulation epochs were observed in animals where recordings were done in a neighboring barrel column in the same or even a different row (n = 3, Fig. 5D), exhibits a striking similarity indicating that lateral cross-columnar inhibition (55) is unlikely the source.”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [55]
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Research works printed but not linked: 1
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Items 101–159 of 159
Devor, A., Boas, D. A., Einevoll, G. T., Buxton, R. B., & Dale, A. M. (2011) · Advances in neurobiology · doi:10.1007/978-1-4614-1788-0_15 · Cited by 16
“Active vasoconstriction could be induced by the release of neurotransmitters or neuropeptides, and may be associated with center-surround electrophysiological patterns of activity consisting of center excitation and surround inhibition (Faraci and Breese, 1993; Faraci and Heistad, 1998; Takashima et al., 2001; Derdikm…”
BackgroundVanni, M. P., Thomas, S., Petry, H. M., Bickford, M. E., & Casanova, C. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0717-15.2015 · Cited by 16
“Dissimilarities in recurrent excitatory and inhibitory circuits within V1 and extrastriate areas could explain these timing differences as observed in the somatosensory cortex (Derdikman et al., 2003; Petersen et al., 2003).”
BackgroundClosed-Loop Systems and In Vitro Neuronal Cultures: Overview and Applications
Bisio, M., Pimashkin, A. S., Buccelli, S., Tessadori, J., Semprini, M., Levi, T., Colombi, I., Gladkov, A., Mukhina, I. V., Averna, A., et al. (2019) · Advances in neurobiology · doi:10.1007/978-3-030-11135-9_15 · Cited by 19
Frostig, R., Chen-Bee, C. H., Johnson, B., & Jacobs, N. S. (2017) · Neurophotonics · doi:10.1117/1.nph.4.3.031217 · Cited by 16
Milliseconds of Sensory Input Abruptly Modulate the Dynamics of Cortical States for Seconds
Deneux, T., & Grinvald, A. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw259 · Cited by 15
“The fast ~150ms evoked response was followed by an initial period of ~750ms, characterized by depolarization (VSD overshoot), and the enhanced firing of a minority of neurons, whereas the rest of the population was silenced, and a fostered rhythmic activity of around 15Hz (Derdikman et al. 2003; Halassa et al. 2011) s…”
BackgroundSelf-citationVersatile networks of simulated spiking neurons displaying winner-take-all behavior
Chen, Y., McKinstry, J. L., & Edelman, G. (2013) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2013.00016 · Cited by 16
“Indirect physiological evidence (Derdikman et al., 2003; Haider et al., 2010) has also been obtained for local excitation and surround inhibition in the cerebral cortex of mammals.”
BackgroundBains, A., & Schweighofer, N. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00433.2013 · Cited by 12
“2011) with net excitatory effects to nearby cells and net inhibitory effects to more distant cells, via connections to local GABAergic neurons (Derdikman et al. 2003).”
BackgroundNakamura, H., Chaumon, M., Klijn, F., & Innocenti, G. M. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm221 · Cited by 14
“Also, the VSD responses did not show a sign reversal corresponding to the negative--positive components of the LFP (as in Grinvald et al. 1994; but see Derdikman et al. 2003).”
BackgroundCholinergic modulation of sensory processing in awake mouse cortex
Jiménez-Martín, J., Потапов, Д. О., Potapov, K., Knöpfel, T., & Empson, R. M. (2021) · Scientific Reports · doi:10.1038/s41598-021-96696-8 · Cited by 18
Goloshevsky, A. G., Wu, C. W. ‐., Dodd, S. J., & Koretsky, A. P. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.04.002 · Cited by 15
Hama, N., Ito, S., & Hirota, A. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2014.08.059 · Cited by 13
Bio-Inspired Networks of Visual Sensors, Neurons, and Oscillators
Ghosh, B. K., Polpitiya, A. D., & Wang, W. (2007) · Proceedings of the IEEE · doi:10.1109/jproc.2006.887320 · Cited by 11
“Such waves have also been described in the primary visual [23], [88] and somatosensory cortices [ 27 ], [36], [72] of mammals, including humans [98].”
BackgroundDubroff, J. G., Stevens, R. T., Hitt, J. M., Maier, D. L., McCasland, J. S., & Hodge, C. J. (2005) · Somatosensory & Motor Research · doi:10.1080/08990220500084990 · Cited by 12
“…between electrophysiological, 2DG, and optical imaging data suggests that the three methodologies are complementary and reveal similar aspects of cortical organization (Derdikman et al. 2003; Hodge et al. 1997; Masino 2003; McCasland et al. 1997; Simons and Land 1987; Takashima et al. 2001).”
BackgroundSong, C., Barnes, S. J., & Knöpfel, T. (2017) · Neurophotonics · doi:10.1117/1.nph.4.3.031214 · Cited by 14
“Later work also confirmed the triphasic response of this elicited activity observed by Kleinfeld and Delaney,(50) a rapid initial depolarization phase, followed by hyperpolarization, and ending with a long-lasting rebound depolarization.(51,53) The stimulus-sensitive hyperpolarizing phase appeared in the form of an as…”
ResultSlow dynamics in features of synchronized neural network responses
Haroush, N., & Marom, S. (2015) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2015.00040 · Cited by 9
“9:40. doi: 10.3389/fncom.2015.00040 Slow dynamics in features of synchronized neural network responses Netta Haroush 1, 2* and Shimon Marom 1, 2 1Department of Physiology, Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel, 2Network Biology Research Laboratories, Faculty of Electrical Engineer…”
InfluentialOmer, D. B., Hildesheim, R., & Grinvald, A. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.045 · Cited by 13
“…et al., 2003; Orbach et al., 1985; Petersen and Sakmann, 2001; Sharon and Grinvald, 2002; Tsodyks et al., 1999) and the somatosensory cortex, (Crochet and Petersen, 2006; Derdikman et al., 2003; Ferezou et al., 2006, 2007; Kleinfeld and Delaney, 1996; Orbach et al., 1985; Petersen et al., 2003).”
Self-citationFast wave propagation in auditory cortex of an awake cat using a chronic microelectrode array
Witte, R. S., Rousche, P. J., & Kipke, D. R. (2007) · Journal of Neural Engineering · doi:10.1088/1741-2560/4/2/007 · Cited by 14
Luo, W., Li, P.-C., Chen, S., Zeng, S.-Q., & Luo, Q. (2007) · Brain Research · doi:10.1016/j.brainres.2006.09.111 · Cited by 12
Adams, B. E. L., Kyi, M., Reid, C., Myers, D., Xu, S.-H., Williams, D. J., & O'Brien, T. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2010.11.001 · Cited by 12
“Rapid imaging technologies now enable higher spatial and temporal resolution of neuronal activity (Berger et al., 2007; Derdikman et al., 2003).”
BackgroundA rat model of somatosensory-evoked reflex seizures induced by peripheral stimulation
Bortel, A. B., Yao, Z. S., & Shmuel, A. (2019) · Epilepsy Research · doi:10.1016/j.eplepsyres.2019.106209 · Cited by 12
MACHINE INTELLIGENCE. ESSAYS ON THE THEORY OF MACHINE LEARNING AND ARTIFICIAL INTELLIGENCE
Шумский, С., & Shumskiy, S. (2019) · Publishing Center RIOR eBooks · doi:10.29039/02011-1 · Cited by 22
Alexander, D. M., Trengove, C., Sheridan, P., & van Leeuwen, C. (2010) · Cognitive Neurodynamics · doi:10.1007/s11571-010-9142-9 · Cited by 12
Devor, A., Trevelyan, A., & Kleinfeld, D. (2007) · Journal of Neurophysiology · doi:10.1152/jn.01218.2006 · Cited by 11
“In complementary work, Devor et al. (2003) measured the intrinsic optical signal in vibrissa S1 cortex of rat, with a stimulus paradigm similar to that in Derdikman et al. (2003), simultaneously with multiple-unit electrical activity.”
BackgroundMethodNeural Computation via Neural Geometry: A Place Code for Inter-whisker Timing in the Barrel Cortex?
Wilson, S. P., Bednar, J. A., Prescott, T. J., & Mitchinson, B. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002188 · Cited by 8
“This model will also explore how stimulus coding might be affected by distance-dependent weights on synaptic connections, as suggested by recent experiments [62,64].”
ResultImaging Vasodynamics in the Awake Mouse Brain with Two-Photon Microscopy
Shih, A. Y., Drew, P. J., & Kleinfeld, D. (2014) · Neuromethods · doi:10.1007/978-1-4939-0724-3_4 · Cited by 14
“Further, the distribution can be dynamically shifted towards regions of heightened electrical activity and concurrent metabolic load [6, 7].”
BackgroundProtosequences in human cortical organoids model intrinsic states in the developing cortexPreprint
van der Molen, T., Spaeth, A., Chini, M., Bartram, J., Dendukuri, A., Zhang, Z., Bhaskaran-Nair, K., Blauvelt, L. J., Petzold, L. R., Hansma, P., et al. (2023) · bioRxiv · doi:10.1101/2023.12.29.573646 · Cited by 9
Chen, G., Carter, R. E., Cleary, J. D., Reid, T. S., Ranum, L. P. W., Swanson, M. S., & Ebner, T. J. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.01.003 · Cited by 11
“Much of this inhibition is GABAergic and generates a center-surround pattern of excitation-inhibition, respectively (Derdikman et al. 2003;Helmstaedter et al. 2009;Fino and Yuste 2011).”
Arzt, M., Sakmann, B. J., & Meyer, H. S. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx156 · Cited by 11
“Transcolumnar projecting INs have been described in L2/3 as well, and were linked to the surround inhibition in the upper layers of the barrel cortex (Kleinfeld and Delaney 1996; Derdikman et al. 2003; Helmstaedter et al. 2008b).”
BackgroundFrancisco, E., Favorov, O. V., & Tommerdahl, M. (2013) · InTech eBooks · doi:10.5772/54801 · Cited by 6
“Single unit studies and imaging studies using voltage-sensitive dyes likewise have shown that excitation in the responding neuronal population is accompanied by the development of a surrounding field of inhibition [32-35].”
BackgroundClomeleon, a Genetically Encoded Chloride Indicator
Berglund, K., Kuner, T., & Augustine, G. J. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-374373-2.00007-8 · Cited by 7
Dynamic spatiotemporal inhibition in the guinea pig auditory cortex
Kubota, M., Sugimoto, S., & Horikawa, J. (2008) · NeuroReport · doi:10.1097/wnr.0b013e32831579ff · Cited by 6
“the magnitude of the hyperpolarization was less than 10% of the magnitude of the early depolarization in the central regions and approximately 25% of that in the surrounding regions [12].”
BackgroundResultTranscranial photoacoustic imaging of NMDA-evoked focal circuit dynamics in rat hippocampus
Kang, J., Kadam, S., Elmore, J. S., Sullivan, B. J., Valentine, H., Malla, A. P., Harraz, M. M., Rahmim, A., Kang, J. U., Loew, L. M., et al. (2020) · Journal of Neural Engineering · doi:10.1088/1741-2552/ab78ca · Cited by 5
Davis, D. J., Sachdev, R. N. S., & Pieribone, V. A. (2011) · Somatosensory & Motor Research · doi:10.3109/08990220.2011.613177 · Cited by 4
“…1990; Ts’o et al. 1990; Kleinfeld and Delaney 1996; Moore and Nelson 1998; Ghazanfar and Nicolelis 1999; Brecht and Sakmann 2002; Brecht et al. 2003; Derdikman et al. 2003; Devor et al. 2003, 2005; Higley and Contreras 2003, 2005; Masino 2003; Petersen et al. 2003a, 2003b; Ferezou et al. 2006,…”
BackgroundResultTwo-Photon Imaging of Cerebral Vasodynamics in Awake Mice During Health and Disease
Summers, P. M., Taylor, Z. J., & Shih, A. Y. (2014) · Springer eBooks · doi:10.1007/978-94-017-9361-2_2 · Cited by 3
“2010), but also allows the dynamic redistribution of blood toward regions of heightened electrical activity (Devor et al. 2007; Derdikman et al. 2003)(Fig.”
BackgroundLuo, W., Li, P.-C., Chen, S., Zeng, S.-Q., & Luo, Q. (2005) · 2005 IEEE Engineering in Medicine and Biology 27th Annual Conference · doi:10.1109/iembs.2005.1616791 · Cited by 4
“Derdikman [11] and Takashima [12] had used the voltage-sensitive dye optical imaging method to observe the phenomena of surrounding inhibition in the rat barrel somatosensory cortex.”
MethodWhisker map organization in somatosensory cortex of awake, behaving micePreprint
Wang, H. C., LeMessurier, A. M., & Feldman, D. E. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/587634 · Cited by 3
Frequency tuning in the rat whisker barrel cortex revealed through RBC flux maps.
Kannurpatti, S. S., & Biswal, B. (2011) · Brain Research · doi:10.1016/j.brainres.2011.08.026 · Cited by 3
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Dynamics of excitability in axonal trees
Cohen, L. D., Galateanu, T., & Marom, S. (2025) · Biophysical Journal · doi:10.1016/j.bpj.2025.11.2682 · Cited by 2
“Briefly, cortices of 0-to 1-day-old rats (Wistar, either sex; Charles River Laboratories) were dissected, dissociated by trypsin treat-ment (T1426; Merck-Sigma Aldrich) and DNase (10104159001; Merck-Sigma Aldrich), followed by trituration using a siliconized Pasteur pipette.”
Extracting grid characteristics from spatially distributed place cell inputs using non-negative PCA
Dordek, Y., Meir, R., & Derdikman, D. (2015) · doi:10.48550/arxiv.1505.03711 · Cited by 2
“The motivation for the use of Mexican-hat like transformations is their abundance in the nervous system [26,27,28].”
BackgroundSelf-citationOptogenetic Sensors for Monitoring Intracellular Chloride
Berglund, K., Wen, L., & Augustine, G. (2015) · doi:10.1007/978-4-431-55516-2_11 · Cited by 2
Neural correlates of perceptual decision-making in the primary somatosensory cortex
Armstrong, A. G., & Vlasov, Y. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2514107123 · Cited by 1
“Can the modulation of epochs 3 and 4 involve surround/lateral inhibition (54) from neighboring barrel columns (55) (Fig.”
Tambaro, M., Guevara, R., Maschietto, M., Leparulo, A., Cecchetto, C., Nicoletti, G., Mariani, B., Suweis, S., & Vassanelli, S. (2025) · bioRxiv · doi:10.1101/2025.07.09.662963 · Cited by 1
“Evidence already exists supporting a functional role of spindle-like oscillations in awake animals, related to whisking 15,18,29–31 .”
Hou, S., Lv, A., Lin, J., You, B., Huang, S., & Song, X. (2025) · AIP Advances · doi:10.1063/5.0244703
Voltage-Sensitive Dye Imaging of Cortical Dynamics
Petersen, C. C. H. (2013) · Neuromethods · doi:10.1007/978-1-62703-785-3_8
Mariani, B., Erra, R. G., Tambaro, M., Maschietto, M., Leparulo, A., Vassanelli, S., & Suweis, S. (2026) · BOA (University of Milano-Bicocca) · doi:10.1371/journal.pcbi.1014521
“To substantiate such a hypothesis, we also recorded neural activity during controlled whisker movements and showed that the frequency centered around 11 Hz is strongly reinforced in the barrel cortex as a response to whisker stimulation [50,54–57].”
Dresbach, S., Gülban, Ö. F., Steinbach, T., Eck, J., Kashyap, S., Kaas, A. L., Weiskopf, N., Goebel, R., & Huber, L. (2026) · Imaging Neuroscience · doi:10.1162/imag.a.1157 · Cited by 1
“Note that the term “triphasic response” has been used for similar signal fluctuations in the animal literature by, for example, Zhu and Connors (1999), Kleinfeld and Delaney (1996), and Derdikman et al. (2003).”
Global and local neuronal coding of tactile information in the barrel cortex
Sharma, H., & Azouz, R. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1291864
Spatio-Temporal Investigation of Brain-Wide SequencesPreprint
Felsenstein, O., & Abeles, M. (2021) · arXiv (Cornell University) · doi:10.48550/arxiv.2105.12976
“, 2005), as well as the somatosensory (Derdikman et al., 2003; Devonshire et al., 2010), and olfactory systems (Cury and Uchida, 2010; Junek et al.”
BackgroundQuintanar-Zilinskas, V. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/621201
“This result is unsurprising, the role of inhibition in sensory cortex input sharpening is well-known(27, 28).”
BackgroundA Rat Model of Somatosensory-Evoked Reflex Seizures Induced by Peripheral StimulationPreprint
Bortel, A., Yao, Z. S., & Shmuel, A. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/506352
Closed-loop control of a modular neuromorphic biohybrid
Keren, H., Partzsch, J., Marom, S., & Mayr, C. (2018) · doi:10.48550/arxiv.1802.07905
Development of a pneumo-tactile vibrissae stimulator for freely behaving rodents
Christ, O., Hofmeier, B., & Hofmann, U. (2017) · doi:10.1007/978-981-10-5122-7_149
Spatiotemporal dynamics in neocortex : quantification, analysis, models
Muller, L. (2014) · theses.fr (ABES) · doi:10.70675/f51645eez86f0z4e55z950cz479373cf87af
“…et al., 1994; Slovin et al., 2002; Jancke et al., 2004; Xu et al., 2007; Ahmed et al., 2008; Han et al., 2008; Nauhaus et al., 2009), somatosensory (Derdikman et al., 2003; Petersen et al., 2003; Civillico and Contreras, 2006), auditory (Reimer et al., 2010); and motor (Rubino et al., 2006)…”
Brain-Based Devices for Neuromorphic Computer Systems
Gall, W. E. (2013) · Defense Technical Information Center (DTIC) · doi:10.21236/ada587348
Representation and Learning in Neuronal Networks: A Conceptual Nervous System Approach
Eytan, D. (2011) · Rambam Maimonides Medical Journal · doi:10.5041/rmmj.10054
Tort, A. B. L. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00039
“The fact that these phenomena are more commonly observed under systemic anesthesia (e.g., Derdikman et al., 2003) than in awake animals (but see Kay, 2005; Tort et al., 2010), makes it tempting to conclude, in light of the above-described work, that awake behavior might suppress both neuronal…”
BackgroundThe influence of GABAergic signaling on dendritic processing
Willadt, S. (2013) · edoc (University of Basel) · doi:10.5451/unibas-006139096
In Vivo Dynamics of the Visual Cortex Measured with Voltage Sensitive Dyes
Rol, P. E., Huang, X., & Wu, J. (2009) · Springer eBooks · doi:10.1007/978-1-4419-0452-2_9
“At some 40 ms after the stimulus start, the whole barrel cortex came depolarized (Kleinfeld and Delaney 1996; Petersen et al. 2003a, b; Derdikman et al. 2003; Civillico and Contreras 2005; Ferezou et al. 2006; Reidl et al. 2007).”
BackgroundInfluential
Metadata
- Authors
- Derdikman, D., Hildesheim, R., Ahissar, E., Arieli, A., & Grinvald, A.
- Affiliations
- Weizmann Institute of Science (IL)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-04-15
- Volume
- 23
- Issue
- 8
- Pages
- 3100-3105
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6742298
- OpenAlex
- W2120250935
- Cited by
- 177
- References
- 33
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 2 · 2023: 1 · 2022: 1 · 2021: 4 · 2020: 2 · 2019: 5 · 2018: 6 · 2017: 6 · 2016: 10 · 2015: 12 · 2014: 9 · 2013: 11 · 2012: 10
- FWCI
- 3.76
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- 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 › Visual perception and processing mechanisms
- Keywords
- surround inhibition, somatosensory cortex, barrel cortex, cortical depolarization, whisker deflection, voltage-sensitive dyes, cortical oscillations, recurrent inhibition, spatiotemporal dynamics, cortical evoked potentials
- MeSH terms
- Animals, Biological Clocks, Diagnostic Imaging, Coloring Agents, Evoked Potentials, Somatosensory, Fluorescence, Male, Models, Neurological, Neural Inhibition, Physical Stimulation, Reaction Time, Somatosensory Cortex, Vibrissae, Normal Distribution, Rats, Wistar, Rats
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