Inhibition-induced theta resonance in cortical circuits

Inhibition-induced theta resonance in cortical circuits Stark Eichler Roux Fujisawa Rotstein Buzsáki

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Inhibition-induced theta resonance in cortical circuits 2013 Neuron 10.1016/j.neuron.2013.09.033 stark2013-inhibition-induced-theta-resonance stark2013-inhibition-induced-theta-resonance.txt, the project's staged copy 3e2f2d38fb962744b52005d7f2dfb6905ee02e06 open-access neuroscience

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0 spans located by searching the stored text for the quote's exact words, allowing any whitespace between them whether the theta-band resonance seen in the membrane potential in vitro appears in the spiking of the same cells in a behaving animal Quotation withheld because this record is not cleared for redistribution. whether and how subthreshold resonance is translated to the spiking regime in behaving animals Quotation withheld because this record is not cleared for redistribution. spiking resonance at theta is not intrinsic to the pyramidal cell but is conferred on it by rhythmic PV inhibition, and it requires HCN currents Quotation withheld because this record is not cleared for redistribution. mechanism Quotation withheld because this record is not cleared for redistribution. theta-band spiking resonance in cortical pyramidal cells Quotation withheld because this record is not cleared for redistribution. electrophysiology electrophysiology Quotation withheld because this record is not cleared for redistribution. mechanisms periodic PV inhibition hyperpolarizes pyramidal cells, activating HCN/Ih channels whose deinactivation produces time-locked post-inhibitory rebound spikes at theta frequency Quotation withheld because this record is not cleared for redistribution. mechanisms rebound spiking of a fixed latency after release from inhibition acts as a band-pass filter on the inhibitory input frequency Quotation withheld because this record is not cleared for redistribution. mechanisms at high input frequencies dense PV spiking tonically suppresses targets while at low frequencies gaps in inhibition let pyramidal cells fire, which alone acts as a low-pass filter Quotation withheld because this record is not cleared for redistribution. mechanisms short-term depression of the inhibitory synapse weakens hyperpolarization at low input frequencies, removing the drive for Ih activation and so suppressing sub-theta rebound Quotation withheld because this record is not cleared for redistribution. mechanisms PV interneurons of the active assembly suppress competing cells, and release from that inhibition triggers rebound spikes that seed the next cell assembly on the opposite theta phase status: the paper's own words: We hypothesize that Quotation withheld because this record is not cleared for redistribution. the inductive effects of the hyperpolarization-activated current create a negative feedback that opposes voltage changes, and that feedback is what creates resonance Quotation withheld because this record is not cleared for redistribution. a low-pass account is available too: dense PV spiking tonically suppresses targets at high frequencies while low frequencies leave windows in which pyramidal cells can still fire Quotation withheld because this record is not cleared for redistribution. HCN alone gives rebound at sub-theta frequencies as well, so a timing mechanism is needed to suppress the low end and turn a low-pass into a band-pass Quotation withheld because this record is not cleared for redistribution. an OLM interneuron released from inhibition just in time can block the low-frequency rebound, which is one way to implement that timing mechanism Quotation withheld because this record is not cleared for redistribution. depression of the inhibitory synapses is the other way: at low input frequencies the presynaptic rate is higher, the synapses depress, and the hyperpolarisation that would drive HCN is reduced Quotation withheld because this record is not cleared for redistribution. PV cells themselves show no frequency preference, which is consistent with basket cells lacking the current that produces it Quotation withheld because this record is not cleared for redistribution. The pharmacological result shows Ih is necessary but not sufficient for theta spiking resonance what this limits: the Ih result: THE PHARMACOLOGICAL EXPERIMENTS ESTABLISHED THE REQUIREMENT OF Ih FOR THETA-BAND SPIKING RESONANCE BUT NOT ITS SUFFICIENCY Quotation withheld because this record is not cleared for redistribution. HCN channels are not the whole story; further mechanisms may sharpen the resonance in intact networks what this limits: the HCN account as complete: further mechanisms may sharpen the resonance in the intact network beyond the CRITICAL ROLE OF HCN CHANNELS the experiments support Quotation withheld because this record is not cleared for redistribution. The proposed assembly-seeding function of rebound spikes is acknowledged as speculative what this limits: the assembly-seeding hypothesis: WHILE SPECULATIVE, THIS HYPOTHESIS IS COMPATIBLE WITH ALL KNOWN OBSERVATIONS ON PUTATIVE BASKET NEURONS Quotation withheld because this record is not cleared for redistribution. the blockade establishes that HCN is required and explicitly not that it is sufficient what this limits: the same scope as limitations[0], with the response: TO INVESTIGATE WHETHER Ih ALONE IS SUFFICIENT, WE CONSTRUCTED A BIOPHYSICAL MODEL Quotation withheld because this record is not cleared for redistribution. further mechanisms beyond HCN are expected to sharpen the resonance in the intact network what this limits: the same scope as limitations[1] - HCN is critical but not the whole mechanism Quotation withheld because this record is not cleared for redistribution. the assembly-seeding account of the rebound spikes is labelled speculative by the authors duplicate of: limitations[2] · what this limits: the same scope as limitations[2] - the rebound-spike account is labelled speculative Quotation withheld because this record is not cleared for redistribution. a gain-baseline correlation is offered with its own artefactual reading, a spiking rate ceiling what this limits: the gain-baseline correlation: PRESUMABLY DUE TO a ceiling on spiking rate, not a property of the circuit (RANK CORRELATION -0.31; n=110; p<0.001) Quotation withheld because this record is not cleared for redistribution. a coherence-baseline correlation is likewise offered as possibly a floor effect, since silent cells cannot be suppressed further what this limits: the coherence-baseline correlation: THIS INCREASED COHERENCE MAY SIMPLY BE A FLOOR EFFECT AS SILENT CELLS CANNOT BE coherent (RANK CORRELATION 0.31; p=0.003) Quotation withheld because this record is not cleared for redistribution. the number of interneurons actually illuminated is an estimate spanning an order of magnitude what this limits: the size of the manipulation: THE WEAK FOCAL PHOTOSTIMULATION AFFECTED AN ESTIMATED 2-20 PV INTERNEURONS, an order-of-magnitude range Quotation withheld because this record is not cleared for redistribution. half the recorded units were classified by waveform rather than by tagging, and low-confidence ones were dropped what this limits: half the recorded units: NON-TAGGED UNITS (692 OF 1413, 51%) ARE CLASSIFIED AS PUTATIVE PYRAMIDAL CELLS (PYR) OR INTERNEURONS (INT) ACCORDING TO WAVEFORM MORPHOLOGY Quotation withheld because this record is not cleared for redistribution. the chirp - a linear frequency sweep - used as a stimulus to read a biological system's frequency response Quotation withheld because this record is not cleared for redistribution. low-pass filter and band-pass filter as the names for the two candidate explanations of the same band-limited discharge Quotation withheld because this record is not cleared for redistribution. the inhibition-induced theta-band spiking reproduced in a pyramidal cell-interneuron model that included the I_h current eliminates: an in-vivo result with no mechanism behind it - the model has only the components the explanation names, so if the effect appears there it does not need anything else · outcome (stated by the tagger, no quotation): held Quotation withheld because this record is not cleared for redistribution. gain gain Quotation withheld because this record is not cleared for redistribution. resonance here is defined generically as amplification in a limited frequency band, which is what lets the same word cover a membrane potential effect and a spiking effect that this paper shows come apart Quotation withheld because this record is not cleared for redistribution. subthreshold and suprathreshold resonance are separate claims: the first is established in vitro, the second is what this paper asks about, and directly-driven pyramidal cells do NOT show the second Quotation withheld because this record is not cleared for redistribution. INT is defined by a NEGATIVE result - interneurons NOT driven by the light - so the class is an outcome of the manipulation rather than a cell type, and the authors say some of them are probably PV cells that the light missed Quotation withheld because this record is not cleared for redistribution. the opsin's specificity and sensitivity are measured separately: every labelled cell was PV, but 10 percent of PV cells were unlabelled Quotation withheld because this record is not cleared for redistribution. a well-isolated unit is defined by three explicit numerical thresholds on amplitude, cluster quality and refractory violations Quotation withheld because this record is not cleared for redistribution. the theta index is a ratio to the cell's own broadband coherence, so it equals 1 under no bias - the measure carries its own null Quotation withheld because this record is not cleared for redistribution. the ZD-index is a normalised difference between control and drug coherence, built so that the drug effect can be shown to be specific to a frequency band and a cell type rather than global Quotation withheld because this record is not cleared for redistribution. claim_type: mechanism a second reading reaching the same value. Recorded: mechanism — note: a second reading reaching the same value from a different sentence. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. method: optogenetic chirp and white-noise stimulation through multi-shank diode-probes with extracellular unit recording, an HCN channel blocker, and a two-cell biophysical model a second reading DIFFERING from the recorded value. Recorded: electrophysiology — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. phenomenon: excess post-inhibitory spiking of pyramidal cells confined to the theta band when PV interneurons are driven rhythmically a second reading DIFFERING from the recorded value. Recorded: theta-band spiking resonance in cortical pyramidal cells — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. builds-on → Zemankovics et al., 2010 (lack of Ih in basket cells) Quotation withheld because this record is not cleared for redistribution. replicates → Stark et al., 2012 (local activation by the light cone of diode-probes) Quotation withheld because this record is not cleared for redistribution. qualifies → the in vitro finding of theta-band subthreshold resonance in cortical principal neurons under intracellular sinusoidal injection Quotation withheld because this record is not cleared for redistribution. builds-on → Cobb 1995's demonstration that basket cell burst discharge induces rebound spikes after release from hyperpolarization in vitro Quotation withheld because this record is not cleared for redistribution. extends → the account of theta generation as a consortium of septal pacemaker, circuit interactions and intrinsic neuronal properties Quotation withheld because this record is not cleared for redistribution. supports → an HCN-mediated mechanism for post-hyperpolarization rebound spiking Quotation withheld because this record is not cleared for redistribution. critiques → the use of grand averages to describe the relationship between pyramidal cells and perisomatic interneurons Quotation withheld because this record is not cleared for redistribution. subthreshold resonance —distinct-from→ spiking resonance subthreshold resonance spiking resonance strength of the relation: 1 · note: THE JOIN HAZARD: one word, two regimes. The paper's own sentence separates them - the subthreshold effect was NOT communicated to the spiking regime, while the spiking effect grew with inhibition Quotation withheld because this record is not cleared for redistribution. PV —causes→ spiking resonance PV spiking resonance strength of the relation: 1 · note: the resonance is conferred by the inhibitory partner, not intrinsic to the resonating cell Quotation withheld because this record is not cleared for redistribution. PV —distinct-from→ INT PV INT strength of the relation: 0.7 · note: CONTAMINATION DECLARED: INT means 'not driven by the light', which is not the same as 'not PV' Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span says a subset of INT MAY be PV cells not activated by light; distinct-from is hedged. Quotation withheld because this record is not cleared for redistribution. I h —causes→ resonance I h resonance strength of the relation: 1 · note: MECHANISM: an inductive negative feedback opposing voltage change Quotation withheld because this record is not cleared for redistribution. HCN1 —part-of→ CA1 HCN1 CA1 strength of the relation: 1 · note: abundant in distal apical dendrites of CA1 AND neocortical layer 5 pyramidal cells - which is why the same effect turns up in both regions Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span says HCN1 channels are abundant in the dendrites of CA1 pyramidal cells; part-of is loose. Quotation withheld because this record is not cleared for redistribution. chirp —contrasted-with→ white-noise chirp white-noise strength of the relation: 1 · note: THE DESIGNED CONTRAST: the same cells get both stimuli, and periodicity is the only thing that differs Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span says responses to chirp and white-noise stimuli were compared; contrasted-with is loose. Quotation withheld because this record is not cleared for redistribution. frequency correlation —contrasted-with→ time correlation frequency correlation time correlation strength of the relation: 1 · note: EACH EQUALS 1 UNDER ONE HYPOTHESIS: two measures constructed so that the rival predicts a specific number, not merely a direction Quotation withheld because this record is not cleared for redistribution. band-pass filter —contrasted-with→ low-pass filter band-pass filter low-pass filter differs in: THE AXIS IS INPUT FREQUENCY, WITH THE MECHANISM GIVEN AT BOTH ENDS. 'Quotation withheld.' The same circuit is one filter or the other depending on the frequency it is driven at, so the two descriptions are not rival claims but the same mechanism at two operating points. · strength of the relation: 1 · note: the two rival accounts are named by the filter each would produce, which is what makes them separable by measurement Quotation withheld because this record is not cleared for redistribution. OLM —causes→ band-pass filter OLM band-pass filter strength of the relation: 1 · note: the timing mechanism that removes the low-frequency rebound HCN alone would produce Quotation withheld because this record is not cleared for redistribution. synaptic depression —causes→ I h synaptic depression I h strength of the relation: 1 · note: SIGN: negative - depression reduces the hyperpolarisation that would drive the current, and it bites hardest at low frequencies Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span says depression REDUCES the hyperpolarization drive to I h activation; the direction is not stated on the edge. Quotation withheld because this record is not cleared for redistribution. theta-index —operationalised-as→ coherence theta-index coherence strength of the relation: 1 · note: the measure is a ratio to the cell's own broadband value, so its null is 1 by construction Quotation withheld because this record is not cleared for redistribution. Kolmogorov-Smirnov test Kolmogorov-Smirnov test Quotation withheld because this record is not cleared for redistribution. permutation test permutation test Quotation withheld because this record is not cleared for redistribution. chi-squared test chi-squared test Quotation withheld because this record is not cleared for redistribution. Mann-Whitney U test Mann-Whitney U test Quotation withheld because this record is not cleared for redistribution. Kruskal-Wallis test Kruskal-Wallis test Quotation withheld because this record is not cleared for redistribution. Wilcoxon signed-rank test Wilcoxon signed-rank test Quotation withheld because this record is not cleared for redistribution. t-test t-test Quotation withheld because this record is not cleared for redistribution. rank correlation rank correlation Quotation withheld because this record is not cleared for redistribution. Poisson test Poisson test Quotation withheld because this record is not cleared for redistribution. Rayleigh test Rayleigh test Quotation withheld because this record is not cleared for redistribution. binomial test binomial test Quotation withheld because this record is not cleared for redistribution. circular-linear correlation circular-linear correlation Quotation withheld because this record is not cleared for redistribution. spectral coherence (multi-taper estimate) spectral coherence (multi-taper estimate) Quotation withheld because this record is not cleared for redistribution. standard error of the mean standard error of the mean Quotation withheld because this record is not cleared for redistribution. linear regression with R-squared linear regression with R-squared Quotation withheld because this record is not cleared for redistribution. permutation test permutation test Quotation withheld because this record is not cleared for redistribution. Kolmogorov-Smirnov test Kolmogorov-Smirnov test Quotation withheld because this record is not cleared for redistribution. rank correlation rank correlation Quotation withheld because this record is not cleared for redistribution. U-test U-test Quotation withheld because this record is not cleared for redistribution. Directly photoactivated pyramidal cells each spiked in a narrow frequency band, but the preferred band differed between cells and across the population covered the whole 0-40 Hz range, i.e. no group-level theta preference. Quotation withheld because this record is not cleared for redistribution. When PV interneurons rather than pyramidal cells were driven with the chirp, pyramidal-cell spiking became coherent with the stimulus specifically in the 4-11 Hz theta band. Quotation withheld because this record is not cleared for redistribution. Nearly half of the light-modulated pyramidal cells fired excess rebound spikes at the trough of the theta-band chirp, with a median firing-rate gain of 3.2 over baseline. Quotation withheld because this record is not cleared for redistribution. Despite strong PV activation, white-noise inhibition frequency-modulated only 0.7% (2 of 271) of pyramidal cells. Quotation withheld because this record is not cleared for redistribution. Resonant pyramidal spiking upon PV activation did not result from adaptation, and required a rhythmic pattern of inhibition. Quotation withheld because this record is not cleared for redistribution. Theta-resonant pyramidal spiking depended on the effective magnitude of local inhibition. Quotation withheld because this record is not cleared for redistribution. Blocking Ih pharmacologically abolished the theta resonance. Quotation withheld because this record is not cleared for redistribution. Pyramidal cells fired at a similar theta phase during chirp PV activation as during spontaneous LFP theta, at the population level. Quotation withheld because this record is not cleared for redistribution. In the model, theta-band resonance was most robust with a timing mechanism that prevented spikes at low frequencies: an OLM interneuron or synaptic depression of the inhibitory synapse. Quotation withheld because this record is not cleared for redistribution. individual PYR tended to spike at narrow frequency bands, but the band differed from cell to cell and at the group level spanned the entire range of tested frequencies Quotation withheld because this record is not cleared for redistribution. driving PV interneurons instead produced band-limited pyramidal spiking confined mainly to the trough of the stimulus Quotation withheld because this record is not cleared for redistribution. the coherence between light and spiking was predominantly in the 4 to 11 Hz theta band Quotation withheld because this record is not cleared for redistribution. 45 percent of light-modulated pyramidal cells rebounded at the theta trough with a median gain of 3.2 Quotation withheld because this record is not cleared for redistribution. TWO RIVAL MECHANISMS ENUMERATED IN ADVANCE, each named by the filter it would produce: tonic suppression giving a low-pass, or rebound giving a band-pass Quotation withheld because this record is not cleared for redistribution. pyramidal cells were less suppressed at low frequencies, which is compatible with the first of the two Quotation withheld because this record is not cleared for redistribution. THE NULL: white-noise activation of PV cells left only 0.7 percent of pyramidal cells frequency modulated Quotation withheld because this record is not cleared for redistribution. FIRST DEFENCE OF THE NULL: overall spiking gain rose during both chirp and white noise, so the stimulation was not ineffective Quotation withheld because this record is not cleared for redistribution. SECOND DEFENCE: white-noise and chirp spiking gains correlated cell by cell at 0.58, so the suppression was not inefficient Quotation withheld because this record is not cleared for redistribution. THIRD DEFENCE: PV cells followed the white-noise stimulus no less precisely than the chirp, so spike following was not impaired Quotation withheld because this record is not cleared for redistribution. white noise in fact suppressed pyramidal spiking MORE strongly than the chirp, 0.28 against 0.49 gain Quotation withheld because this record is not cleared for redistribution. the conclusion the three defences license: periodic inhibition, not inhibition as such, is what creates spiking resonance Quotation withheld because this record is not cleared for redistribution. TWO MEASURES BUILT SO EACH EQUALS 1 UNDER ONE RIVAL: frequency correlation is 1 for a purely frequency-dependent unit, time correlation is 1 for a purely adapting one Quotation withheld because this record is not cleared for redistribution. frequency correlation was 0.19 and 0.32 and significant, while time correlation was 0.054 and 0.02 and largely not Quotation withheld because this record is not cleared for redistribution. so the resonance is not adaptation, and a rhythmic inhibition pattern is required Quotation withheld because this record is not cleared for redistribution. theta preference grew with the strength of PV activation, while subthreshold resonance never reached the spiking regime even at low direct drive Quotation withheld because this record is not cleared for redistribution. theta resonant pyramidal spiking depends on the effective magnitude of local inhibition Quotation withheld because this record is not cleared for redistribution. under chirp PV activation cells spiked near the stimulus trough, the same phase relationship they show during spontaneous theta Quotation withheld because this record is not cleared for redistribution. blocking HCN abolished the theta preference of pyramidal but not PV spiking, at population and single-unit level Quotation withheld because this record is not cleared for redistribution. DRUG SPECIFICITY SHOWN, NOT ASSUMED: synaptic transmission survived the infusion, since PV activation still silenced pyramidal spiking Quotation withheld because this record is not cleared for redistribution. NECESSITY ESTABLISHED AND SUFFICIENCY EXPLICITLY NOT: the blockade shows HCN is required, and a model was built to ask whether it is enough Quotation withheld because this record is not cleared for redistribution. THE MODEL REFUSED TO CONFIRM: HCN alone produced rebound at sub-theta frequencies too, and only an added timing mechanism made the resonance theta-specific Quotation withheld because this record is not cleared for redistribution. PV cells followed light up to 40 Hz with no frequency preference, consistent with basket cells lacking the current Quotation withheld because this record is not cleared for redistribution. the disagreement with in vitro work is attributed to the preparation: synaptic activity present in vivo, and the depolarising rather than hyperpolarising drive Quotation withheld because this record is not cleared for redistribution. the current is largely deactivated near spike threshold, which is offered as why directly depolarised cells showed no theta resonance Quotation withheld because this record is not cleared for redistribution. membrane resistance is much lower in a waking animal than in vitro, which may let neurons follow higher input frequencies Quotation withheld because this record is not cleared for redistribution. ARTEFACTUAL READING OFFERED BY THE AUTHORS: the negative gain-baseline correlation is attributed to a spiking rate ceiling Quotation withheld because this record is not cleared for redistribution. AND AGAIN: the positive coherence-baseline correlation may simply be a floor effect, since silent cells cannot be suppressed further Quotation withheld because this record is not cleared for redistribution. the opsin was fully specific but not fully sensitive: every labelled cell was PV, and 90 percent of PV cells were labelled Quotation withheld because this record is not cleared for redistribution. 1413 units were recorded, 1151 classified as pyramidal, 240 as interneurons and 22 left unclassified Quotation withheld because this record is not cleared for redistribution. resonance resonance Quotation withheld because this record is not cleared for redistribution. theta-index theta-index Quotation withheld because this record is not cleared for redistribution. ZD-index ZD-index Quotation withheld because this record is not cleared for redistribution. spiking gain spiking gain Quotation withheld because this record is not cleared for redistribution. frequency correlation frequency correlation Quotation withheld because this record is not cleared for redistribution. resonance resonance Quotation withheld because this record is not cleared for redistribution. theta-index theta-index Quotation withheld because this record is not cleared for redistribution. ZD-index ZD-index Quotation withheld because this record is not cleared for redistribution. INT INT Quotation withheld because this record is not cleared for redistribution. frequency correlation frequency correlation Quotation withheld because this record is not cleared for redistribution. cell type cell type Quotation withheld because this record is not cleared for redistribution. chirp direction chirp direction Quotation withheld because this record is not cleared for redistribution. light intensity light intensity Quotation withheld because this record is not cleared for redistribution. spiking gain spiking gain Quotation withheld because this record is not cleared for redistribution. baseline rate baseline rate Quotation withheld because this record is not cleared for redistribution. coherence coherence Quotation withheld because this record is not cleared for redistribution. gain gain Quotation withheld because this record is not cleared for redistribution. theta-index theta-index Quotation withheld because this record is not cleared for redistribution. 33% (101/309) — locally stimulated pyramidal cells directly activated by light in CaMKII::ChR2 mice, versus 59% (108/184) of interneurons in PV::ChR2 mice Quotation withheld because this record is not cleared for redistribution. 50/110 (45%) — light-modulated pyramidal cells showing rebound spiking at the theta chirp trough; median gain 3.2 Quotation withheld because this record is not cleared for redistribution. 0.7% (2/271) — pyramidal cells frequency-modulated by white-noise PV activation Quotation withheld because this record is not cleared for redistribution. 1413 — total units recorded in chronic animals: 1151 pyramidal, 240 interneurons, 22 unclassified Quotation withheld because this record is not cleared for redistribution. 142±13 spikes/sec — mean firing rate of directly driven PV interneurons during chirp photostimulation Quotation withheld because this record is not cleared for redistribution. 0.19±0.04 and 0.32±0.04 — frequency correlation between ascending and descending chirp coherences (CaMKII and PV mice), against time correlations of 0.054±0.04 and 0.02±0.05 Quotation withheld because this record is not cleared for redistribution. 0.49±0.09 — pyramidal-cell spiking gain during chirp PV activation versus 0.28±0.07 during white-noise PV activation Quotation withheld because this record is not cleared for redistribution. 0.52 — rank correlation between same-shank interneuron theta peak gain and pyramidal-cell chirp coherence, across all pyramidal cells Quotation withheld because this record is not cleared for redistribution. 9.8±0.9 Hz — peak resonance frequency of CA1 pyramidal spiking under PV chirp activation before Ih blockade Quotation withheld because this record is not cleared for redistribution. 121/257, 47% — pyramidal cells significantly modulated by the chirp during direct CaMKII stimulation, versus 27/46 (59%) of interneurons Quotation withheld because this record is not cleared for redistribution. 4–11 Hz — the theta band in which coherence and excess spiking are concentrated Quotation withheld because this record is not cleared for redistribution. 50/110 (45%) — share of light-modulated pyramidal cells that rebounded at the theta trough Quotation withheld because this record is not cleared for redistribution. 0.7% (2/271) — pyramidal cells frequency-modulated under white-noise PV activation - the null Quotation withheld because this record is not cleared for redistribution. 0.19±0.04 and 0.32±0.04 — frequency correlations, against time correlations of 0.054 and 0.02 Quotation withheld because this record is not cleared for redistribution. 100% and 90% — all 84 EYFP+ cells were PV+, and 84 of 93 PV+ cells were EYFP+ Quotation withheld because this record is not cleared for redistribution. 2–20 PV interneurons — estimated number of cells the focal light actually reached Quotation withheld because this record is not cleared for redistribution. 692 of 1413, 51% — units classified by waveform rather than by tagging Quotation withheld because this record is not cleared for redistribution.

The full text of this article is not redistributable, so it is not included here. The evidence sentences are withheld with it; the tag layer and its grounding status remain. The article itself is at https://doi.org/10.1016/j.neuron.2013.09.033.