Journal of Physiology control alone (see Buzsáki, 2002 for review). relationship which is in difficult to explain to excitatory and inhibitory inputs has the timingofhippocampal output activity campus (King impose a coherent theta frequency oscillation on the hippo- doubt on the notion that the MSDB alone has the capacity cast to have MSDB the concerning findings recent However, MSDB. from inputs so, more and, activity cholinergic on formation hippocampal the in observed frequencies theta at activity of majority The Buzsáki cortex and other subcortical structures (Petsche entorhinal the (MSDB), Broca of band medial septum-diagonal the from inputs rhythmic between interactions have been variously proposed to originate from reciprocal experiments, lesion from and, formation hippocampal the of areas all in prominent are oscillations frequency Theta 1989). Buzsáki, 1986; Lynch, & (Larson retrieval and formation memory of models in and 1978) Nadel, & including processing of visuospatial information (O’Keefe processes cognitive various in implicated been have and are readily observed in the hippocampal formation Hz) (4–12 frequencies theta at oscillations potential Field Physiology and Pharmacology, SUNY Health Science Center, Brooklyn, NY 11203, USA School of Biomedical * Sciences, University of Leeds, Leeds LS2 GlaxoSmithKline, 9NQ, Harlow, UK, Essex, † CM19 5AW, * Depa UK and ‡ Whittington A. M. and * *, ‡, *, E. †, *, F. R. M. H. T. C. E. D. J. Buhl Gloveli H. N. Traub Gillies Davies LeBeau hippocampal area CA1 A model of atropine-resistant theta oscillations in rat © The Physiological Society 2002 Journal of Physiology et al. 1983; Vertes & Kocsis, 1997). interneurons controlling electrogenesis in pyramidal cell apical dendrites. be can oscillations generated theta as a population consequence of that intrinsic theta suggest frequency spiking We activity in trains. a subset of IPSP stratum oriens frequency theta and theta field both of loss a by accompanied was interneurons these in spiking of Disruption oscillations. theta-frequency intrinsic demonstrating interneurons temporally oriens stratum all in spiking were with activity correlated interneuron pyramidale stratum and firing burst Pharmacological dendritic IPSPs. IPSPs, faster smaller, of trains by modulation of IPSPs altered the followed theta oscillation suggesting an inhibitory network origin. Somatic kinetics slow with IPSPs withinitial potentials synaptic inhibitory compound of consisted oscillations theta showed responses burst spiking and were temporally related to trains of IPSPs with slow kinetics. Pyramidal somatic dendritic apical distal pyramidal with co-expressed were oscillations theta Field areas. ammonic AMPA receptor activation. This activity occurred in the absence of inputs from area CA3 and extra- population theta atropine-resistant oscillations in response generates to metabotropic glutamate CA1 receptor activation under area conditions of reduced hippocampal that demonstrate We hippocampus. the in activity rhythmic of feature predominant a are oscillations frequency Theta S 9NL, UK. LS2 author Corresponding (Resubmitted 20 May 2002; accepted after revision 2 July 2002; first published online 19 July 2002) (2002), et al. 543.3 1998). In addition data demonstrating , Email: [email protected] pp. 779–793 in vivo in M. A. Whittington: School of Biomedical Sciences, The Worsley Building, University of Leeds, Leeds Leeds, of University Building, Worsley The Sciences, Biomedical of School Whittington: A. M. appears dependent appears revealed a complex terms of extrinsic with reference et al. in vivo 1962; hs rcpos n te MA utp o glutamate of subtype NMDA the and receptors these (e.g. van Hooft metabotropic glutamate receptor (mGluR)-dependent drive to sensitive differentially are interneurons Hippocampal laminae and the moleculare 2002). dentate gyrus lacunosum (Buzsáki, and oriens ammonis cornu in specific involvement of a number of interneuron subtypes trains of spikes from fast-spiking interneurons and suggested rhythmic with activity, interneuronal inhibitory of amount large a by accompanied are oscillations frequency theta (Fisahn frequencies theta at activity weak only with band, gamma the within is CA3 area in the most robust form of oscillation generated by carbachol (Traub genesis vivo & Kauer, 1997). However, in this form of model, unlike by attenuated AMPA receptor blockers are (MacVicar & Tse, they 1989; Williams where CA3, area in particularly discharges, theta-like generate to bicuculline) without or (with carbachol of application used has work this of Most range. theta the within activity rhythmic generate of number situations in which a the hippocampal formation alone may demonstrated have slices hippocampal vitro In itrern ciiy s o esnil o rhythmo- for essential not is activity interneuron , oes f ht feuny siltos in oscillations frequency theta of models et al. et al. et 2000), and positive interactions between 1992). With inhibition intact, by far by intact, inhibition With 1992). DOI: 10.1113/jphysiol.2002.024588 et al. et 1998). www.jphysiol.org In vivo In rtment of in , Journal of Physiology atropine, 10 CaCl 20 1 gkg mg (10 ehl popii ai) 1 acid), phosphinic methyl) (3,4-dichlorophenyl)ethyl]amino-2-hydroxypropyl](phenyl- O % 95 humidified and ACSF oxygenated between interface the 450 campus, (Scientific Procedures)Act1986.Transverseslicesofmidhippo- Animals UK the with accordance in out carried were procedures All sucrose. of concentration equiosmolar an with replaced been tetrahydrobenzo[f]quinoxaline-7-sulfonamide), 20 tetrahydrobenzo[f]quinoxaline-7-sulfonamide), rptsimaeae(eitne6–0 M or potassium acetate (resistance 60–100 methylsulfate potassium either containing microelectrodes glass using USA) CA, City, Union Inc., Instruments, (Axon amplifiers Axoclamp via made were recordings Intracellular kHz). Hz–2 (0.1 M 3 < (resistance ACSF containing microelectrodes amplifiers glass using UK) Neurolog (Digitimer, via made were recordings Extracellular transverse slices between CA3 and CA1 subfields. hnllcn) 20–200 phenylglycine), (( DHPG concentrations: known at applied ( soma the of level the at recorded of injection depolarising current on ( generation burst and action AHPs amplitude small potentials, low their by 200 identified > were and impaled pyramidale were dendrites neuronal ( accommodation current little depolarising with on injection rates firing fast and AHPs brief large, their electrophysiological properties and demonstrated brief spikes, in homogeneous more were interneurons pyramidale Stratum membrane potential oscillationsintheabsenceofdrugapplication( frequency theta intrinsic and (AHPs) polarisations afterhyper- compound large, potentials, action brief showed The data presented are from a subset of oriens interneurons which characteristics. electrophysiological diverse demonstrated neurons fluid (ACSF, containing (m ro t ijcin f eaie >10m kg mg 100 (> ketamine of injection to prior g) were Male fully Wistar anaesthetised rats with (~150 isoflurane METHODS or abolished. oscillations whenAMPAreceptoractivationisattenuated also frequency receptors theta inhibition-based, prominent, generates glutamate metabotropic of activation (Whittington blocked is activation receptor AMPA when oscillations area CA1 of the hippocampus generates gamma frequency transient of extrinsic, phasicinputs.Wehavepreviouslyshownthat devoid hippocampus the in oscillations frequency mGluR activationmayalsoplayaroleingeneratingtheta (Cobb hippocampus the in oscillations frequency theta metabotropic cholinergic receptors has and been reported to generate robust mGluRs of co-activation addition (Awad reported been have 1983) Leung, genesis theta for critical receptor 780 m 2 5% CO –5 M 2 2; MgSO , ; AP5 ( AP5 ; et al. et m activation of metabotropic glutamate receptors in receptors glutamate metabotropic of activation _1 2 ), then cardioperfused with artificial cerebrospinal artificial with cardioperfused then ), m D t3 C A minislices were obtained by dissecting °C. CA1 at 35 M m thick, were cut horizontally and maintained at maintained and horizontally cut were thick, m -(_)-2-amino-5-phosphonopentanoic acid), 50 acid), -(_)-2-amino-5-phosphonopentanoic 2000). From this it was hypothesised that hypothesised was it this From 2000). et al. 4 ; bicuculline, 30 2; NaHCO , V ). Potentials were band pass filtered on-line filtered pass band were Potentials ). 1995). Herewedemonstratethat n 7). In addition pyramidal cells = were also m M M NQ (2,3-dioxo-6-nitro-1,2,3,4- NBQX ; 3 :NC,16 C,3; NaH ): NaCl, 126; KCl, , 24; glucose, 10) in which NaCl had m m M M ; CGP55845 ((2 daea, 1–10 diazepam, ; n in vivo in = 25). All drugs were bath were drugs All 25). = n V ) Aia pyramidal Apical 3). = ). Stratum oriens inter- (Vanderwolf & (Vanderwolf m et al. et _1 S fo stratum from m )-3,5-dihydroxy- ad xylazine and ) S m M )-3-[[(1 2000). In 2000). ; carbachol, ; 2 PO M. J. Gillies and others in vitro in m M 4 tonic and ; , 1.25; n S 11). = )-1- M m ; ie esrmns ol ol b etmtd wn t the to owing estimated be compound nature of only the inhibitory events. could measurements time Decay analysis. the in used slice each from measured were IPSPs 600 than More Inc.). (Synaptosoft Minianalysis using measured right of the central peak of the correlograms. IPSP rise times were the the to peaks positive first measuring and negative first the between distance by calculated were values Correlation signals. intracellular and potentials field pyramidale recorded stratum concurrently from data of epochs s 3 of correlograms signal. Average spike timing electrode profiles were quantified by combining cross intracellular and potential field pyramidale stratum recorded concurrently of superimposition by illustrated were timing spike of Patterns activity. recorded of epochs s 60 of kHz) from digitised power data spectra (digitisation frequency 10 Peak frequency of recorded activity was determined off-line from or Sigma (Poole, UK). (20–200 DHPG of application bath by slices hippocampal rat of Gamma frequency oscillations were generated in area CA1 theta frequency oscillation AMPA receptor blockade transforms gamma into RESULTS pa i pwr pcr o 3 9 ± 37 of spectra power in peak a SYM2206 (10 SYM2206 campal slices ( hippo- intact with compared slices CA1-only in different significantly not was band theta the in power peak Mean shown). not (data removed surgically were inputs hilar band was also apparent in CA1 mini-slices where CA3 and HG ln pa pwr ihn h tea ad n area in band theta the within power peak alone DHPG of shown presence the In as 1989). Tse, & NBQX (MacVicar previously of application bath on oscillations blockade, but were attenuated concurrently with gamma CA3 compared with CA1 in the absence of AMPA receptor Theta frequency oscillations were 1 more prominent in area (Fig. CA3 area in rhythmogenesis of pattern the to theta of expression frequency field oscillations in area CA1 was in stark contrast blockade-dependent AMPA The thiopental, 50 nrae rm2 7 ± increased from22 Hz). Peak power the power in the upper theta band (6–12 gamma band ( (1.0–1.5 rqec f3 Hz ( 2 ± frequency of 37 ihr eky r o a al Fg 1 (Fig. application of NBQX (20 all at not or weakly either frequencies theta at modulated were oscillations gamma rqece Fg 1 theta (Fig. frequencies at rhythmicity clear ( Hz demonstrated 0.3 correlations ± 6.7 of frequency peak mean application of carbachol (20–40 bath with seen were CA1 area in oscillations theta field of expression blockade-dependent receptor AMPA Similar auou mlclr ad te lmne Fg 1 (Fig. laminae other and moleculare lacunosum radiatum/ stratum distal between reversal phase clear m m M M ). Stratum pyramidale field recordings showed ad h seii AP rcpo blocker receptor AMPA specific the and ) m M P m P . Drugs were obtained from Tocris (Bristol, UK) M 0.001, < 0.19, = ) (data not shown). Activity in the theta the in Activity shown). not (data ) A ). Laminar profiles ( profiles Laminar ). m n V n n 6). = 2 m 29) and increased dramatically = 29). In each case the resulting = M Hz ) abolished field power in the _1 m o15±43 ± to 115 M ) and NBQX or kainate m A V . oee, bath However, ). 2 n Hz n = 4) revealed a revealed 4) = J. Physiol. m _1 9. Auto- 29). = V t mean a at 2 Hz _1 543.3 C at a y B -axis ). ). Journal of Physiology receptor suggested an essential role of GABA of role essential an suggested receptor The above data on the effects of drugs acting on the GABA IPSPs are compartmentally distributed ( GABA some by modified were oscillations theta field Atropine-resistant Hz ( 0.2 ± with AP5, 4.8 Hz; 0.4 ± 8.5 (control, frequency peak lower significantly remaining in the presence of carbachol and AP5 showed a ( (10 atropine antagonist receptor acetylcholine muscarinic the to resistant were in the absence of AMPA receptor-mediated fast excitation The field theta frequency oscillations generated by DHPG atropine resistant and involve inhibition mGluR-induced theta frequency oscillations are 30 ± 115 was CA3 ht feunis ( frequencies theta diazepam (1 ( i.2 Fig. 6±42 (carbachol ± reduced 76 significantly also were oscillations NMDA receptor antagonist AP5 (50 AP5 the antagonist receptor NMDA of application bath by modified differentially were and glutamatergically generated theta frequency oscillations J. Physiol. GABA ( often compound IPSPs with similar rise times were still were times rise similar with IPSPs compound often AMPA receptor-mediated fastexcitation smaller trainsof 3 (Fig. ms 2.2 around times rise estimated of distribution tight a with time, IPSPs were fairly homogeneous both in amplitude and rise 1±12 ± 41 peak frequency or amplitude of oscillation ( . 0.8 ± 9.2 ( Hz 0.3 ± 7.5 4±2 ± 14 oe ihDP a 5±9 ± power with DHPG was 45 theta (peak AP5 with abolished almost were oscillations infcnl rdcd n h peec o atropine of presence the (control in CA1 reduced area significantly were which NBQX, in of presence the in carbachol, generated with oscillations theta-band to in 2 the presence of atropine (Fig. 9±11 ± 19 odtos ht pwr a 4 10 ± 45 was power theta conditions n n to a barrage of fast GABA membrane potentials fluctuate at gamma frequencies owing 3). During gamma (Fig. oscillations pyramidal cell somatic neurons pyramidal CA1 from recordings intracellular frequencies. This was investigated further using somatic theta at rhythmogenesis in inhibition synaptic mediated rsne f G585 hs au ws 7±6 ± 37 was value this CGP55845 of presence P n 8, = 5, = )i otosad4 11 ± 7) in controls and 45 = .5 wtot fetn pa apiue ( amplitude peak affecting without 0.05) < Bb B m P P receptor antagonistCGP55845(1 ). Thiopental (50 m m V m 543.3 > 0.05). Bicuculline almost abolished power at power abolished almost Bicuculline 0.05). > .5 Fg 2 Fig. 0.05, < V 2 m V V ek oe 9 41 ± 96 power peak 2 Hz V 2 2 m Hz 2 Hz Hz M Hz _1 n _1 , _1 _1 ( n ) O adto o NQ ti fl to fell this NBQX of addition On 4). = A _1 n ( n n abco P 0±19 ± 40 AP5 + carbachol and 6) significantly reduced peak = frequency eetr ouaos bt o b the by not but modulators, receptor t ma feuny f . . Hz 0.5 ± 7.3 of frequency mean a at 5, = ( P P 5, = m 0.05). < V 0.05, < P P Aa C 2 P m A < 0.05). Muscarinic AchR-driven Muscarinic 0.05). < 0.05). < Hz . fe cmlt bokd of blockade complete After ). m .5 i.2 0.05, Fig. < receptor-mediated IPSPs. These . oee, ht oscillations theta However, ). M M . en ek mltd was amplitude peak Mean ). _1 ) had no significant effect on m n V m t ma feuny of frequency mean a at , i.2 Fig. 6, = m 2 V Ab V Hz 2 2 Hz ). This was in contrast Theta oscillations in hippocampal area CA1 Hz _1 m Ab ihDP AP5 + , with DHPG _1 M _1 m ). Cholinergically ). mGluR driven mGluR ). ( P wt atropine with , V m n 2 0.05, > Ba M 7, = Hz ). Incontrol , whereas ), A _1 m P P m receptor- i the in , V V 0.05; > n 0.05) > 2 2 6). = Hz Hz _1 _1 A as s, 50 bars: 1 traces show field potentials from CA1 stratum pyramidale. Scale field gamma oscillation into a field theta oscillation. Example as indicated. electrode in stratum pyramidale and a roving electrode positioned cross s) correlations using (_0.5 two to electrodes: 0.5 a reference sharp phase reversal in distal stratum radiatum. Data shown are administration. differences in the field oscillation before and after NBQX power within the theta band. Autocorrelations show frequency 20 power in both gamma and theta bands. Bath application of NBQX oscillations in area s CA3. epochs, Power spectra (60 Blockade of AMPA receptors with 20 the effects in area CA1. A receptors exposes theta field oscillations driven by metabotropic 1. Reduction in Figure AMPA receptor-mediated drive , DHPG, 20–200 m M leaves only a small peak at theta frequencies in contrast to m C, .Pwrseta(0s V. epochs) Power show spectra large (60 increase in DHPG, 20–100 B, m laminar profile of theta field potentials reveals a M , generates gamma oscillations in area CA1. m M , generates gamma/theta m M NBQX transforms the n 5) show = 781 Journal of Physiology receptors with bicuculline (30 attenuated by NMDA receptor blockade. A, NBQX generated by DHPG and carbachol, in the presence of 2. Pharmacology of Figure theta field oscillations 782 mAchR activation. range ( frequency of the oscillation and enhanced power in the lower theta n atropine (10 of theta activity generated by mGluR activation in the presence of text). reduced theta power during mAchR-mediated oscillation (see theta band for mGluR-mediated oscillations and significantly whereas blockade of GABA ( mGluR-mediated theta oscillations. Bath application of 50 n 4) had no effect. = both mGluR and mAchR mediated theta oscillations are 5) for theta oscillations = generated by DHPG or carbachol. Ab n , mean power spectra ( 7) whereas thiopental had = no significant effect ( m M ) and abolition of theta activity generated by B, Bb effects of GABA receptor modulators on m , diazepam (1 MD B -AP5 almost abolished power in the receptors with CGP55845 (1 m n M 5) showing slight enhancement = ) abolishes theta activity ( Ba m , blockade of GABA M ) reduced the mean peak Aa , mean power spectra M. J. Gillies and others m n M A n 6). = , =6) 01 A idcd oi frn a tea frequencies theta at 4 firing (Fig. tonic induced nA) +0.15 to (+0.05 current depolarising of injection case each In potential. membrane resting at interneurons above the Spiking was seen spontaneously but sporadically in each of M mV 5 5 ± ± and 40 _59 input of oscillations and theta field potential during resistance membrane theta-generating a 11 had remaining interneurons The study. the from theta membrane intrinsic no with cells spiking Fast alveus. the to close oriens stratum of one-third outer the in impaled in the population theta-band activity observed. Cells were activity oscillatory frequency theta intrinsic demonstrating below) we examined the role of stratum oriens interneurons (see oscillation theta field the of profile pharmacological and 6 3 mV (Figs dendrites were artificially depolarised to _30 oscillations theta during IPSPs slower these of presence the revealed 200 (> recordings dendritic slow the and kinetics suggested a possible broad dendritic origin. Distal apical was seen times rise of range The ms. 5 field ± pyramidale potential peak was stratum 12 and IPSP peak between lead phase strongly 3 were correlated withconcurrentfieldrecordings(Fig. and frequencies theta at occurred IPSPs slower These ms. 6 ± 27 were oscillations theta field during estimated decay time constants for the slower IPSPs visible during decays field IPSP oscillations. gamma during seen those than longer also were IPSPS slower these of times mV). Estimated decay cells from six slices recorded at _30 ms ( 1.7 larger IPSPs having slower, ± a mean the of for 6.5 values the with bimodal was oscillations theta-band ms. field during 0.6 times rise ± of distribution 2.2 were The oscillations gamma during IPSPs seen those than aduring longer times rise with seen also was seen at gamma frequencies but an additional class of IPSP Lcil, 99 Maccaferri 1999; Lacaille, & mid- and distal-pyramidal cell apical dendrites (Chapman generating of intrinsic theta capable frequency firing patterns with projections are to interneurons) moleculare area within interneuron inhibitory of subtypes two least At hyperpolarisation-activated current interneurons are associated with inhibition and Theta frequency oscillations in stratum oriens triggered averaging showed a theta frequency pattern of pattern frequency theta a showed averaging triggered 4 (Fig. frequencies theta at pattern firing robust mV and induced a 3 ± an average resting potential of _53 20 m M CA1 (oriens lacunosum-moleculare and lacunosum and lacunosum-moleculare (oriens CA1 gamma oscillations were 15.2 ± 3.1 ms, whereas the whereas ms, 3.1 ± 15.2 were oscillations gamma B oscillation impaled in this region ( A NBQX) tonically depolarised these interneurons to ). ). Bath application of 50 uegmaoclain(i.3 (Fig. oscillation gamma pure and V , respectively. during field gamma oscillations when oscillations gamma field during m m from stratum pyramidale) stratum from m m t al. et M DHPG (or DHPG and n 00. ie the Given 2000). C 3) were rejected = (I ). Rise times for times Rise ). P h ) J. Physiol. 0.05, < A B ). Mean ). Spike ). n 543.3 =6 B Journal of Physiology J. Physiol. 543.3 shown as 600 mean individual distributions IPSPs for per > recording ( observed in somatic and distal apical dendritic compartments during gamma or theta field oscillations. Data ms. 100 (Ic), mV 5 ms. Scale bars: 100 are negatively correlated with the local field potential with a phase lag of 4–6 Hz). IPSP trains at theta frequency 4, frequency rhythmic 4–11 trains of IPSPs with slower kinetics (see Fig. as expressed also are oscillations Theta traces). (lower lag/lead phase no show and potential field local the with correlated negatively are trains IPSP Hz). 35–60 (frequency kinetics fast with IPSPs of train rhythmic a as expressed are oscillations Gamma respectively. NBQX, + DHPG and DHPG by induced oscillations A, gamma and field field during frequencies theta theta oscillations at active are dendrites apical distal cell Pyramidal 3. Figure cl as V(3 V,1 V(6 V,10ms. 100 mV), (_65 mV 10 mV), (_30 mV 5 bars: Scale theta at IPSPs of trains show frequencies also and complex dendrites fast spike events distal at theta frequencies oscillations at more hyperpolarised theta membrane potentials. field/somatic During spikes. broad mV) 3 ± more negative membrane potentials theta oscillations are observed as trains of small amplitude (6 field/somatic gamma mV. oscillations At demonstrate rhythmic Hz) IPSPs at at _30 theta frequencies (3–10 ocret A srtm yaiae il ad oai itaellr eodns f am ad theta and gamma of recordings intracellular somatic and field pyramidale stratum CA1 concurrent B, itlaia edii eodns( 250 (> recordings dendritic apical distal Theta oscillations in hippocampal area CA1 C, histograms of distribution of IPSP rise times rise IPSP of distribution of histograms m m from stratum pyramidale) during pyramidale) stratum from m n 4 in each condition). > m V (field), 783 Journal of Physiology the by a hyperpolarising activated current. Bath application of possibility that tonic firing was maintained, at least in part, was ( current injection negative of presence continued the in decayed hyperpolarisation this However, spiking. of cessation and nA current produced to a _0.2 transient hyperpolarisation polarisation of recorded interneurons by Hyper- injection of _0.1 frequencies. theta at output strong a revealed s epochs) action potential generation and power spectra (60 784 urn i te rsne f D28 etrd pkn in spiking these cells restored but rhythmicity ZD7288 was absent. of presence the in current 4 all (Fig. abolished spiking spontaneous and interneurons of hyperpolarisation I h etrd fe 35s Fg 4 (Fig. s 3–5 after restored blocker ZD7288 (10 t . . ad ht feuny spiking frequency theta and s 0.3 ± 1.5 = oriens interneurons is disrupted by ZD7288, 10 spectrum of 60 epoch of data from a cell during depolarising current injection as in 0 ms. 100 s. mV, 0.5 nA currentinjection.Scale bars:50 mV)andduring+0.1 _56 = at restingmembranepotential(RMP and as 0m,05s. mV, 0.5 Scale injection. current nA bars: 50 +0.1 during and mV) _59 = (RMP potential membrane resting at interneuron Aa 4. Stratum oriens Figure interneurons generate theta frequency spiking 0m,05s. mV, 0.5 50 mV) nA hyperpolarising current injection following _54 recovery of and spiking during (see _0.1 results). Scale bars: = (RMP potential membrane resting at interneuron oriens one from data show traces Example in cl a:10ms. Scale bar: 100 siig n res nenuos n h asne f rg Eape rcs hw aa rm n oriens one from data show traces Example drug. of absence the in interneurons oriens in spiking , Aa Cb Cb and . Cc , spike triggered averages of 20 consecutive periods during injection of +0.1 nA current. Scale bar: Scale current. nA +0.1 of injection during periods consecutive 20 of averages triggered spike , , power spectrum of 60 epoch of data from a cell during depolarising current injection as in as injection current depolarising during cell a from data of epoch 60 of spectrum power , Ab Bb . m Ba , spike triggered averages of 20 consecutive periods during ms. RMP. Scale bar: 100 M C Ac , spiking in oriens interneurons in the presence of DHPG, 50 DHPG, of presence the in interneurons oriens in spiking , ) mV) produced a small (2–3 Ab ). Injection of depolarising of Injection ). , power spectrum of 60 epoch of data from a cell during depolarising current injection as , spike triggered averages of 20 consecutive periods nA during current. injection of +0.1 Ba . hs ugse the suggested This ). M. J. Gillies and others m M . Example traces show data from one oriens interneuron am-rqec ipt Fg 5 (Fig. inhibitory input the gamma-frequency despite frequencies theta at only fired but active tonically were DHPG interneurons oriens these alone, of the presence the In in pyramidale. injection, current stratum of absence of level the at gamma field oscillation local the to antiphase in appeared approximately trains IPSP that showed correlations Cross 5 (Fig. frequency gamma at IPSPs received interneurons During field gamma oscillations, induced by DHPG, these seen as potential field local the with correlated temporally tightly were activity theta-band field during interneurons 5 Fig. (autocorrelations, manner precise temporally more a in but frequencies theta at potentials action fire to continued interneurons oscillations for pyramidalIPSPs(meanphaseleadIPSPpeak Ba m M and and NBQX, 20 NBQX, and Bb . B Ca B ). IPSP trains in these in trains IPSP ). . uig il theta field During ). spiking in , Bc power , m Ca M . J. Physiol. 543.3 A ). Journal of Physiology J. Physiol. 543.3 bars: 100 Scale IPSPs. frequency theta of abolition complete almost demonstrate interneurons) (five slices five from data pooled from spectra Power potential. membrane mV _30 at recorded interneurons onto IPSPs slow eoaie nuos t 3 V Sae as 01m (il) 5m ( mV 5 (field), mV 0.1 bars: Scale V. _30 at neurons depolarised NBQX). Intracellular recordings taken from artificially + oscillation (DHPG) and theta oscillations (DHPG A, 5. Theta activity Figure in stratum oriens interneurons uoorlgas eel oe htmc ht siig uig il tea hn uig il gamma field during than theta field during ms. spiking 200 mV, theta 10 bars: Scale oscillations. rhythmic more However, clarity. reveal for truncated spikes autocorrelograms cases, membrane both resting in frequencies at theta oscillations at NBQX) occurs spiking + Note potential. (DHPG theta and (DHPG) gamma during interneurons in correlograms showing phase relationship between interneuron IPSPs and field theta oscillations. concurrent stratum pyramidale field potential and intracellular interneuron recordings during gamma during recordings interneuron intracellular and potential field pyramidale stratum concurrent m fed,1 mV ( V (field), 10 Theta oscillations in hippocampal area CA1 I c 3 V,20ms. mV), 200 _30 C, 10 m M ZD7288 blocks both field theta oscillations and trains of trains and oscillations theta field both blocks ZD7288 I c 3 V, 0 s Blw r cross are Below ms. 200 mV), _30 B, spiking 785 Journal of Physiology 786 recorded stratum pyramidale field potentials. field pyramidale stratum recorded and Overlaid oriens traces from nine consecutive stratum theta periods aligned with both the peak upward deflection with in concurrently correlate temporally IPSPs stratum pyramidale interneuron somatic spiking Compound 6. Figure bursts of action potentials during the descending phase of the field theta oscillation. utbfr,o uig ekuwr elcini h il eodn seas i.3 Fig. also (see recording field the in deflection upward peak during, or before, just to theconcurrently recordedfield( the and interneurons oscillations in pyramidal cell soma in the absence of current pyramidale injection reveal compound IPSPs phase locked stratum in generation potential action beginning of action potential of generation in oriens end theta interneurons. the towards period a oscillation. theta field the of phase rising Ca initial the on potentials action single generated interneurons orlto) cl as 0m,6 mV ( ms, correlation). 60 Scale bars: 20 pyramidal cell nA soma , depolarising (injected current) with generated 0.2 single action potentials within D ). Theinitialpeaks oftheIPSPsaremarkedwith arrowsandoccurred A , M. J. Gillies and others B , Ca ,2mV ( ), 2 A, stratum radiatum, fast spiking, interneurons generated interneurons spiking, fast radiatum, stratum Cb ,04mV ( ), 0.4 D Cb ). , subthreshold membrane potential B, stratum oriens theta A right panel cross panel right J. Physiol. 543.3 Journal of Physiology Lacaille, 1999). In addition to testing the role of theta generators (Maccaferri & McBain, 1996; Chapman & subclass of oriens interneuron, but not in LM-interneuron has been shown to disrupt spike generation in the ‘O-LM’ 3 relationship forIPSPsinpyramidalcellsFig. ( ms 4 ± stratum 11 the was field pyramidale in deflection upward peak to compared Disruption of the hyperpolarisation-activated current hyperpolarisation-activated the of Disruption shown). not (data dendrites apical neuronal pyramidal in those seen to similar kinetics estimated having components individual with events inhibitory compound of consisted J. Physiol. il gma siltos ( oscillations gamma field xmnd h efcs n il tea siltos Bath oscillations. application of ZD7288 theta (10 field on effects the examined also we (above), interneurons oriens theta-generating 543.3 ahapiaino . m bath application of 0.1 traces show a train of spikes at theta frequency recorded at mV a before membrane and potential after of _68 ciiy cl as V 0 ms. mV, activity. 100 Scale bars: 5 frequency. Blockade of field theta and dendritic electrogenesis with Ni edie.Saebr:5m,10ms. mV, 100 dendrites. Scale bars: 5 A, on dendritic electrogenesis dependent is NBQX and DHPG by generated oscillations theta field of Expression 7. Figure iklin 01m nickel ions (0.1 m M n ) had no significant effect on , aa o son but shown) not data 5, = M ) block both distal dendritic spike generation and the field theta oscillation. Example n ,Fg 5 Fig. 5, = M Theta oscillations in hippocampal area CA1 Ni 2+ . Power spectra show abolition of field theta power and theta activity in distal B, A , cf. phase cf. , depolarisation of distal dendrites reveals trains of slow IPSPs at theta A I ). They h in the I h rpris f hs itrern wr ciia t the to critical generation of CA1 population were theta oscillations. interneurons these of properties 5 These data suggested that intrinsic (Fig. theta frequency spiking itself oscillation theta field the abolished and abolished the theta frequency pattern of pyramidal IPSPs, oetas n tau prmdl itrern a a at interneurons pyramidale stratum in potentials action of Trains 5). Fig. Hz, 0.1–15 at filtered pass (band potential field pyramidale stratum recorded concurrently the to aligned temporally were interneurons oriens and cells pyramidal interneurons, pyramidale stratum from during field theta frequency activity. Intracellular recordings above described interneurons generating theta oriens in and stratum pyramidale interneurons relative to the activity neurons pyramidal of relationships firing the examined We oscillations Action potential timing during theta frequency 2+ failed to alter theta-frequency IPSP C 787 ). Journal of Physiology 788 interneuron output. Scale bars: 20 ms, 5 mV (dendrite), 30 mV (oriens interneuron), 0.3 mV (field). mV 0.3 and interneuron), (oriens timing mV IPSP B, 30 (dendrite), the mV between 5 ms, relationship the 20 bars: Scale illustrate output. interneuron to potential) field recorded concurrently the 7 also Fig. (see burst previous the of onset the after ms 62–71 peaking IPSPs by prolonged AHP Note positivity. field the peak upward deflection of the field to demonstrate to aligned are correlation Traces Hz). between dendritic burst 0.1–15 pass (band firing recording field pyramidale and stratum concurrent with dendrite somatic A, 8. Timing of Figure dendritic bursts is controlled by IPSPs depolarising current injection (0.1–0.3 nA) into dendrites disrupted dendritic burst timing in a manner a in timing burst dendritic disrupted dendrites into nA) (0.1–0.3 injection current depolarising dendritic spike-triggered average of five periods of a theta oscillation recorded in a pyramidal apical pyramidal a in recorded oscillation theta a of periods five of average spike-triggered dendritic A ). Five consecutive periods of oriens interneuron activity are also superimposed (and aligned to M. J. Gillies and others J. Physiol. 543.3 Journal of Physiology fired interneurons single action potentials with a phase lead of oriens Stratum field. pyramidale stratum the cf. leads phase of range broad a with potentials action fired interneurons pyramidale Stratum potential. field with a fixed phase angle compared to peak str. pyramidale were strongly correlated with the field theta oscillation but pyramidal neuronal somatic membrane potential changes The above sequence of spikes and IPSPs demonstrated that through dendritic electrogenesis Field theta frequency oscillations are expressed ( ms 9 ± 24 of spiking cell oriens of lead phase mean a demonstrated pyramidale stratum of level the at oscillation theta field and firing cell theta theta oriens stratum 6 in interneurons (Fig. spike single a of generation the with temporally corresponded firing interneuron pyramidale stratum of Cessation activity. frequency theta field of periods 0.92 per generated spike one least at with number of 6 spikes per theta period ranged from zero to (Fig. five oscillation theta field the of descending phase the on seen were Hz 45–80 of frequencies was shown to abolish the field theta band oscillations. interneurons oriens from outputs rhythmic of abolition However, electrode. recording extracellular the by up directly responsible be for the observed field potential not picked could interneurons and neurons pyramidal in suggested that the pattern of membrane potential changes the observations These field. before pyramidale stratum the of ms peak 10–15 peak to seen were cells pyramidal and interneurons oriens in seen IPSPs slow large, the and 9, Discussion). Fig. (see potentials action of trains generated interneurons pyramidale str. when period the during IPSPs smaller appear IPSPs these of tail The generation. potential action cell theta oriens after ms 10 approximately negativity seen on the upward phase of the field neuronal soma revealed compound IPSPs with initial peak membrane potential oscillations at the level of the pyramidal 6 (Fig. cells theta oriens approximately concurrentwiththefiringofaspikeinstr. end ofthetrainstr.pyramidaleinterneuronspikesand the towards i.e. oscillation, period field the of trough the theta during field per spike one fired cells pyramidal nA). In these conditions tonic depolarising current (0.1–0.2 of injection with elicited be could but recorded cells 1/25 only in seen was firing somatic cell Pyramidal peak. field J. Physiol. 543.3 pe rcs,04mV (field, upper lower traces), traces). 0.4 mV (dendrite, ms, 10 dual periodicity corresponded with the two peaks in the power spectra. Scale bars: 60 current injection induced burst firing on the tail of the previous burst AHP before IPSP onset. The resulting recorded apical potentials dendrite. pyramidale stratum from panel) concurrently with dendrites (right showed no change in field theta power on depolarisation of a single pyramidal spectra from spectra field in Mean peak split dendrites. Note depolarised (control). without and (depol.) depolarisation with experiments from ( data show spectra power Mean prolongation. AHP IPSP-mediated of breakdown with consistent B ). Cross correlation of stratum oriens Ca ). Analysis of the subthreshold the of Analysis ). C, example traces illustrate the effect of depolarisation on dendritic burst firing. Depolarising n ) oprd with compared 5) = Theta oscillations in hippocampal area CA1 A prolonged by prolonged . n oscillation = 3). The 3). = ca 5ms 25 transmission significantly. Bath application of Ni not did nickel that demonstrated also authors These 2002). and voltage-dependence to those seen here (Isomura kinetics origin, spatial similar of spikes calcium dendritic abolish selectively to shown been have ions Nickel intact. IPSPs frequency the theta recorded intracellularly leaving of pattern while oscillation field the abolish should of the field theta frequency oscillation then their blockade expression the for responsible were spikes dendritic these If oscillations. frequency theta field radiatum stratum distal in troughs axis 1 dendritic (Fig. apical the along oscillation theta field (data not shown), i.e. because of the phase reversal of oscillation the field pyramidale stratum the of peak the with ms ( 7 of ± difference +3 phase mean a showed correlations Cross oscillation. field local the with correlated strongly were 3 Fig. cf. fsnl rdul pkso ogrdrto Fg 7 (Fig. duration longer a of spikes double or single of those seenduringgammaoscillationsandoftenconsisted from modified were oscillations frequency theta during seen spikes The frequencies. theta small at spikes generated amplitude mV _60 and _70 between potentials membrane at dendrites oscillations theta and gamma field both During electrogenesis: dendritic pyramidal involve to appeared answer The occur. could oscillations discrepancy apparent between the timing of interneuron outputs and field theta this how investigated next We edii siig hwd h cret spatiotemporal origin the for candidate a considered be to characteristics correct the showed spiking dendritic nickel-sensitive that indicated observations above The Dendritic periodicity involves both AHPs and IPSPs Fg 7 activity (Fig. theta during spikes these abolished completely rqec rne n il rcrig ( recordings field in theta range the frequency in power of abolition complete almost an by input to pyramidal cells at theta frequencies was not. on pyramidal dendritic electrogenesis, the pattern of inhibitory dependent was oscillations theta field of expression 7 (Fig. frequencies theta at mV revealed a persistence _30 of inhibitory synaptic input in pyramidal cell dendrites. Depolarisation of dendrites to oscillation did not affect the trains of slow IPSPs recorded However, abolition of dendritic spiking and the field theta fet oai brtn, o dd t fet synaptic effect it did nor bursting, somatic affect B ) dendritic spikes corresponded temporally to the to temporally corresponded spikes dendritic ) B A ). During theta oscillations these dendritic spikes ). Ablation of dendritic spiking was accompanied was spiking dendritic of Ablation ). n 5) when comparing peak dendritic = positivity B ) suggesting that, although that, suggesting ) n P =5) 0.05, < 2+ 01m (0.1 n et al. 5). = A 789 , M ) Journal of Physiology occurred after a small IPSP which occurred in time with 8). With non-depolarised spiking dendrites (Fig. spiking dendritic accompanying the and oscillations theta field spectra ( AHP. power the mean comparing when seen was by this for Evidence control towards and IPSP the by control from away spikes dendritic of generation of pattern the dendritic spike before IPSP invasion then this should shift sequence. If this depolarisation were sufficient to AHP–IPSP initiate a the in earlier generation spike for threshold reach to dendrite the allow should current of injection by dendrite recorded the of depolarisation then case the was AHP, but on the more rapid rebound from the IPSP. If this spikes previous the of rebound slow the on not generated were spikes dendritic Thus burst. dendritic a following (AHP) afterhyperpolarisation intrinsic the prolong to We hypothesised that the slow dendritic IPSPs were acting the timing of dendritic spikes. in role a played IPSP dendritic the than other factors that 8 (Fig. wave polarising potential changesbetweenspikesrevealedabiphasichyper- membrane dendritic subthreshold of analysis However, spikes. dendritic the and field pyramidale stratum the of peak the before ms fired 25 approximately potentials action interneurons these and ms), (20–30 interneurons seen were for IPSPs that appeared to originate from oriens (Whittington oscillations controlled was by the periodicity kinetics of network and IPSPs (unlike synchrony gamma theta local that unlikely seemed it spikes/ model this In dendritic activity. band of theta population timing the and frequency theta a discrepancy left between the timing of interneuron outputs at still this However, oscillation. theta field the of 790 n 5) of concurrently recorded = stratum pyramidale A f loFg 7 Fig. also cf. , et al. et 1995)). The slowest kinetics slowest The 1995)). A ). This suggested This ). M. J. Gillies and others local population theta frequency oscillation. the to reference with spiking dendritic the of periodicity depolarisation in individual pyramidal cells controlled the dendritic of degree These the that indicate interneurons. also observations oriens by generated apparently IPSPs dendritic from rebound the on occurring spiking is temporally coordinated by the network IPSP input, with 8 the theta frequency IPSP (Fig. and AHP the from decay to corresponding one and AHP spike the from decay spike to corresponding one generation, for periodicities two in resulted depolarisation field 8 concurrent (Fig. the faster to and compared slower when at frequencies occurring peaks bimodal with nA) the spectrum peak was split depolarised (+0.1 to +0.2 and 8 and atthesamefrequencyas,fieldoscillation(Fig. with, coordinated temporally occurred spiking dendritic 8 (Fig. output interneuron oriens the GABA and receptor NMDA on dependent strongly drive, receptor rhythm which was independent of muscarinic cholinergic 2002). The pharmacology of this field oscillation revealed a Buzsáki, Hz; (2–5 theta atropine-sensitive for seen that not but rat, awake the in observed that to corresponded range frequency This Hz). (6–10 band high-theta the in frequency a with oscillation field a generates preparation receptor activation in area CA1 of glutamate the hippocampal slice metabotropic that demonstrate data These DISCUSSION oscillation by pyramidal cell dendritic electrogenesis. stratum pyramidale field potential. corresponding to the peak downward deflection in the positivity (i.e. towards the end of the train of small IPSPs) action potentials at the peak of the membrane potential occurred but injection of depolarising current generated pyramidal somatic action potential generation rarely in stratum pyramidale interneurons. Spontaneous IPSPs temporally correlated with action potential generation electrogenesis and is terminated by a train of small, faster depolarising hump temporally correlated to dendritic interneuron firing. This is then interrupted by a small IPSP temporally correlated with the period of oriens ‘theta’ change. The compound IPSP consists of an initial, large, Hz) and pyramidal somatic 0.1–15 membrane potential stratum pyramidale field potential (band pass filtered period of theta oscillation with concurrently recorded burst firing in apical dendrites. The figure shows a single pyramidale and stratum oriens ‘theta’ interneurons, and potential generation in pyramidal cell soma, stratum Schematic representation of the procession of action electrogenesis somatic compound IPSP and neuronal 9. Relationship between Figure pyramidal cell C . oee, hn h rcre dnrts were dendrites recorded the when However, ). B A ). Analysis of dendritic recordings showed that showed recordings dendritic of Analysis ). receptor activity and expressed as a field potential C ). Thus dendritic spiking A ). In this mode this In ). J. Physiol. 543.3 B Journal of Physiology theta radiatum in this model is also seen with ‘atropine resistant’ stratum mid in seen change phase sharp the example For ht seen that trough in stratum pyramidale field potentials also matches of the with sparsity) correspondence general its (and spiking cell pyramidal the and interneurons fast-spiking CA1 area in seen those match model reduced this in oscillations frequency theta of properties the of Many theta frequencies. not appear to impose their activity on an ‘inert’ network at for the observation of theta activity in area CA1 Buzsáki (Petsche regions extra-ammonic from inputs rhythmic Thus, region. brain this to intrinsic networks generating theta of existence the for evidence provides system reduced anatomically and pharmacologically a such in all at occur oscillations theta population that fact the Also, intact). excitation receptor-mediated AMPA (with the in intracellularly dendritic compartment even during field gamma observed oscillations were oscillations theta However, rhythms. theta during CA1 area in processing useful a as model Cobb 1989; Tse, & (MacVicar region target the was CA3 where oscillation clearly theta of models was previous to situation different This activity. theta population this see to needed conditions experimental the of ment require- critical a was receptors AMPA of blockade The frequencies. theta at invasion IPSP dendritic of pattern the preserved ions nickel as with electrogenesis dendritic this arrangement of blockage reciprocal a be to not demonstrated of stratum pyramidale apical dendrites. However, this was provide to activity electrogenic appeared rhythmic the to organisation temporal frequency theta at interneurons these in generation potential action coherent mission, trans- synaptic excitatory fast receptor-mediated AMPA of blockade During model. present the in cells pyramidal in and interneurons these in both trains IPSP frequency (Maccafferi & McBain, 1996) and markedly disrupts theta of pattern intrinsic action their disrupt to shown been has of Blockade interneurons. oriens stratum of subset a in oscillations potential membrane frequency theta intrinsic involve to appeared model this in activity population frequency theta of generation of mechanism key The for thetaoscillations reported than model this in spiking interneuron oriens and separation was seen between pyramidal interneuron spiking Harris Leung, 1983), and field theta oscillations have been & shown (Vanderwolf receptor NMDA the of antagonists by resistant theta oscillations J. Physiol. in vivo et al et et al. potential generation in some oriens interneurons oriens some in generation potential et al. 543.3 .1995; Williams & Kauer, 1997), and limits the limits and 1997), Kauer, & Williams .1995; n vivo in (Buzsáki 2000). However, a greater degree of temporal 1983; Vertes & Kocsis, 1997), though critical in vitro in (Fox in vivo et al. t al. et in vivo tool with which to study signal study to which with tool 1986). The pattern of activity in (Csicsvari 96 Bragin 1986; also appear to be blocked Theta oscillations in hippocampal area CA1 et al. 1999). Atropine t al. et et al. et in vivo in vitro in in vivo in 1995; 1962; , do I . h active al. generating interneurons described by others (e.g. Banks theta proposed to correspond may and 1999) Lacaille, & shown to generate theta frequency oscillations (Chapman Lacunosum moleculare (LM) interneurons have also been 1996; T. Gloveli & E. H. Buhl, unpublished observations). McBain, & (Maccaferri cells bistratified and cells (OLM) moleculare lacunosum oriens – properties generating theta intrinsic have to shown been have interneurons dendrite-targetting oriens stratum of types two least At dipole in area CA1. frequency theta a express to large too was activity gamma field perisomatic models, during present the in oscillations ‘on-going’ gamma was activity frequency theta Traub abolishing field gamma oscillations (see Fisahn receptor blockade in the AMPA present experiments, thus almost by attenuated is which inhibition perisomatic of barrage this is It soma. the at seen as events dendritic dendrite dynamically, thus disrupting the fidelity of distal the of constant length the change to expected be would soma the and origin of site distal the between dendrites origin and soma. A barrage of gamma-frequency IPSPs on of site between compartments dendritic the of properties cable the on dependent be will IPSP the of expression the soma, the to IPSPs dendritic of propagation passive a Assuming 2002). Buzsáki, (see shunting perisomatic via activity dendritic isolate functionally oscillations) targetted inhibitory synapses (as seen during field gamma perisomatically from inputs large that suggest 3) and partmental specificity of gamma and theta rhythms (Figs com- 1 the showing observations present the addition, In et al. (Kamondi electrogenesis dendritic by accompanied be to reported (Buhl reported input inhibitory perisomatic of profile the than distally & McBain, 1996) and appear to target apical dendrites more (Maccaferri ZD7288 to sensitive is that generation potential action demonstrate interneurons OLM 4). (see model Fig. present the the by in demonstrated role major oscillations a play not may so and oscillations by these oriens interneurons was suggested by their firing their by suggested was interneurons oriens these by oscillations theta field of generation the for role critical A bath application of ZD7288 did. whereas cells pyramidal in trains IPSP frequency theta of activity with nickel ions appeared not to affect the pattern However, we demonstrated here that blockade of dendritic due to direct effects on pyramidal dendritic electrogenesis. the effects of ZD7288 on field theta oscillations may also that be possibility the therefore, exclude, cannot We 1998). it istonicallyactiveatrestingmembranepotentials(Magee, been reportedtobepresentinpyramidaldendriteswhere 2000). However, these cells were not reported to require 1998). I et al. et h currents to generate intrinsic theta frequency theta intrinsic generate to currents 2000). This suggested that, though dendritic though that, suggested This 2000). et al. et 1994; Papp 1994; et al. et 2001). et al. I h has also has 1998; et 791 Journal of Physiology may generate Ni generate may cells pyramidal CA1 of compartment dendritic the that Kamondi (e.g. oscillations theta shaping or generating in role a play to A number of dendritic calcium channels have been suggested yaia sie iig n ecttr ad inhibitory and inputs excitatory during theta and timing spike pyramidal go somewaytowardsexplainingthediscrepancybetween spiking). This system, as apparent from present data, may small IPSPs (i.e. approximately in antiphase with dendritic of train this of tail the at spikes generated depolarisations small but model theta this during generation potential action no almost showed recordings somatic Pyramidal recorded. interneurons pyramidale stratum spiking fast of barrage small a to owing prolonged is IPSP the of decay of the stratum pyramidale field). Following this the apparent temporally tothegenerationofdendriticspikes(thepeak of theseIPSPsadistinct‘hump’isoftenseencorresponding cells during one theta period. During the initial decay phase the mean action potential generation time for oriens theta after ms 6 approximately began IPSPs somatic these that was IPSPs these of time rise mean the that Given oscillation. field the of period one of peak form of an initial large ms IPSP before peaking the some 12 somatic IPSPs seen during field theta oscillations took the compound The 9). (Fig. spiking interneuron pyramidale neuronal pyramidal somatic and both dendritic IPSP profiles and fast spiking stratum to respect with relationship 792 (e.g. see Magee see (e.g. activation ofT-type(orP/Q)calciumchannelsindendrites indicated spikes these of profile electrophysiological pharmacological and The oscillation. theta field a during frequency oscillations showed a compartmental profile compartmental a showed oscillations frequency membrane potential oscillations at theta frequency. Theta intrinsic possessing interneurons oriens stratum of subset a theta oscillations recorded atropine-resistant resembled rhythm theta population a population theta exposed oscillation in all CA1 laminae. excitation The resulting glutamatergic receptor-mediated dendritic oscillationsinpyramidal cells.BlockadeofAMPA intracellular frequency theta generated slice hippocampal the of CA1 area in activation mGluR I type summary, In cell activity with behaviour and may be involved in the dynamic changes in pyramidal inputs entorhinal with expected be would depolarisation Such 2001). Magee, also (see depolarisation dendritic to sensitive exquisitely was oscillation, theta population the to The timing of individual pyramidal dendritic spikes, relative in synaptic plastic processes occurring at theta frequencies. field potential, a of theta rhythmogenesis but as may also play a expression, role the to critically contribute only (Ito stimulation theta-burst by induced plasticity synaptic block et al. et IPSPs which temporally correlated with the trains of 1995) suggesting that these dendritic spikes not spikes dendritic these that suggesting 1995) et al. et et al. et 2+ in vivo -dependent spikes at theta frequencies theta at spikes -dependent 1998). Here we have demonstrated have we Here 1998). 1995). Ni 1995). seBzái 2002 for (see discussion). Buzsáki, in vivo in vivo 2+ (O’Keefe & Recce, 1993). and may be generated by has also been shown to shown been also has ca 6 ms this suggested this ms 6 M. J. 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