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Journal Club

Editor’s Note: These short,critical reviews of recentpapers in the Journal , written exclusivelyby graduate students or postdoctoral

fellows, areintended to summarize theimportant findings of thepaper andprovide additional insight andcommentary. For moreinformation on the format and purpose of the Journal Club, please see http://www.jneurosci.org/misc/ifa_features.shtml.

Broadband Spectral Change: Evidence for a MacroscaleCorrelate of Population Firing Rate?

Kai J. MillerNeurobiology and Behavior, University of Washington, Seattle, WA, 98195

Review of Manning et al.

IntroductionIn 1972, Brindley and Craggs measuredthe electric potential from the surface of the baboon brain using a 1-mm-diameterelectrode. They found that the power inthe 80–250 Hz frequency range of theelectric potential time series was dynami-cally increased in motor areas duringmovement.Sites2 mm apart from onean-

other were specific for different move-ments of the same limb. This observation,that power in the high-frequency portionof the brain surface electric potential wasspecific for local cortical activity, wasagain demonstrated in electrocorticogra-phy (ECoG) by Crone et al. (1998) for dif-ferent functions in distant regions of thehuman brain. Both groups proposed thatthis high-frequency power was a correlateof specific cortical activity, but it was un-clear what this power increase meant atthe neuronal level. More recently, Miller

et al. (2009a,b) proposedand demonstratedthat these observed high-frequency powerchanges actually reflected “broadband”power spectral change, across all frequen-cies. The low-frequency portion of thesebroadband changes was often obscured at

lower frequencies by coincident changesin rhythmic phenomena (e.g., and ),so that only the high-frequency portionof the broadband change was observed.These broadband changes have a partic-ular form (a power law in the frequency domain) (Fig. 1) and capture function-ally specific cortical activity with a tem-poral precision of tens of milliseconds

(Miller et al., 2009a,b). A recent Journal of Neuroscience  article by Manning andcolleagues (2009) directly shed light onthe neurophysiologic nature of thesebroadband changes by measuring whataspects of the power spectral density (PSD) of the local field potential (LFP)correspond with single-neuron firingrates measured at the same cortical site.

Manning and colleagues (2009) per-formed the following experiment: in thecourse of treatment for epilepsy, pene-trating microwires were transiently im-

planted in 20 human patients during theclinical identification of seizure foci.Each patient participated in a spatialnavigation task while single-neuron ac-tion potential (AP) firing rates and thesurrounding LFPs were measured froman array of microwires throughout dif-ferent brain sites. The firing rate of eachneuron and the corresponding normal-ized PSD of the LFP were calculated inhalf-second epochs. For each epoch, thepower in the PSD was extracted in fivediscrete frequency ranges: delta (2–4

Hz), theta (4–8 Hz), alpha (8–12 Hz),beta (12–30 Hz), and gamma (30–150Hz). In addition, an estimate of the

broadband power in the PSD, across allfrequencies, was obtained from each ep-och. The firing rate was then comparedwith each power spectral feature using aregression approach, and an associatedsignificance level was estimated by resa-mpling (randomly time-shifting the LFPand AP event times with respect to oneanother to obtain a surrogate distribu-

tion). The best predictor of firing ratewas the broadband feature of the PSD.There is a clear relation between in-creased firing rate and increased broad-band power in the LFP [Manning et al.(2009), their Figs. 1 and 2]. This relationwas robust, significant, and reproducedacross a large number of individuals andbrain sites. Manning and colleagues(2009) experimentally demonstrated,for the first time, that broadband spec-tral change in the electric potential iscorrelated with neuronal AP firing rate.

In the same week that the article by Manning et al. (2009) was published,Whittingstall and Logothetis (2009)published an article showing that 30–100 Hz aspects of the LFP are significantpredictors of multineuron firing rate; itis likely that this high-frequency changereflects a broadband change and repre-sents a secondary confirmation of thefinding by Manning et al. (2009). Theelectrical potential from both studieswas measured at the spatial scale of theLFP, which has recently been demon-

strated to reflect neuronal activity within 250  m of the recording elec-trode (Katzner et al., 2009). Because this

Received Dec. 27, 2009; revised Jan. 20, 2010; accepted Jan. 21, 2010.

K.J.M. is supported by the National Aeronautics and Space Administra-

tion Graduate Student Research Program and the National Institutes of 

Health-National Institute of General Medical Sciences Medical Scientist

Training Program. I thank Dora Hermes and Teresa Esch for reading of this

manuscript.

Correspondenceshouldbe addressedto KaiJ. Miller, Neurobiologyand

Behavior, University of Washington, Allen Building, Box 352350, Seattle,

WA, 98195. E-mail: kjmiller@u.washington.edu.DOI:10.1523/JNEUROSCI.6401-09.2010

Copyright © 2010 the authors 0270-6474/10/306477-03$15.00/0

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broadband spectral change is correlatedwith the action potential rate at the LFPscale, broadband electric potential spec-tral changes may generically representmean firing rate at larger scales as well.If true at larger scales, then the spatialscale that the recording electrode re-

flects would then dictate the size of theneuronal population that the firing rateis being averaged over. Seen in this light,the article by Manning et al. (2009) pro-vides empirical evidence that broadband(or associated high-frequency) changesobserved at larger spatial scales, in ECoG,are a correlate of the mean firing rate of the neuronal population beneath eachrecording electrode.

How might the reader gain intuitionfor the measured correlation in terms of neurophysiology? From a modeling per-spective, heuristics for the relationshipbetween changes in action potential rateand broadband, power-law, changes canbe constructed relatively simply. Proper-ties of the physiology underlying the cur-rent source density (CSD) in differentcortical lamina were established experi-mentally in the late 1970s and early 1980s(Mitzdorf, 1985). Propagating actionpotentials in axons and axon terminalsdoes not contribute strongly to the CSDat spatial scales of   50 to   300   m,e.g., the scales where CSD varies, LFPspool from, or macroscale ECoG poten-

tials average over. Instead, dendriticsynaptic current influx and efflux mod-ulate the CSD and, by extension, the LFPand the ECoG-scale potential. Emergingin vivo, simultaneous recordings of intracellular potential and LFP by Okunet al. (2009) show that the LFP andsingle-neuron transmembrane poten-tialare tightly coupled temporally, inde-pendent of the spiking pattern of theneuron. This implies that the correla-tion observed by Manning et al. (2009)likely reflects the postsynaptic influence

on many neighboring neurons by theneuron whose action potential times arebeing measured, and this may very wellbe augmented by redundant firing pat-terns across neighbors.

A very simple model for producingbroadband spectral changes from changesin firing rate can be illustrated to provideintuition for this correlation, and also toillustrate why the experimental findings of Manning et al. (2009) provide evidencefor a macroscale correlate in populationfiring rate. A model based on original re-

search by Bedard et al. (2006) (laterextended in Miller et al., 2009b) showshow the time course of the intracellular

dendritic charge concentration mightresult from spatiotemporal summationof postsynaptic current influxes fromeach arriving AP (Fig. 1). The broadbandin the PSD results from the noise-like dis-tribution of AP arrival times, and its 1/f falloff with frequency results from theshape of the synaptic current decay and

the effect of temporal integration in thedendritic arbor. The Manning et al.(2009) finding supports models of this

type, where basic phenomena, firing ratechanges, produce spatially larger scalefield potential changes. Furthermore, thestrong correlation between firing rate andbroadband spectral change in the electri-cal potential demonstrated empirically by Manning et al. (2009) provides powerfulevidence that broadband power spectral

changes observed at larger spatial scalesmay be a generic correlate of mean popu-lation firing rate.

Figure 1.   A heuristic model for how broadband spectral increases might emerge from increases in presynaptic AP firingrate.  A, Poisson-distributed presynaptic APs arrive at a neighboring neuron. The PSD of these AP events over time has a

flat, frequency-independent form (i.e., a “white noise” shape, with spikes coming with equal probability at every fre-quency; blue trace in G ).  B, At the synapse between the two neurons, each arriving AP triggers release of a neurotrans-mitter and postsynaptic current influx. As shown in the central schematic neuron, this results in a gradient of chargedensity within the dendritic arbor.  C , The temporal shape of the postsynapti c current smears out the PSD, giving i t a 1/f 2

form, with a “kink” at a particu lar frequency determined by the decay time,  , of the postsynaptic current (here 70 Hz),

shown with a gray arrow in  G . D , In this model, the inputs from 6000 su ch synaptic currents are integrated over time andspace, simulating the time-dependent change in transmembrane charge concentration. The associated transmembranepotential produces a time-dependent current across the dendritic membrane.  E , The combined effect of synaptic andtransdendritic current influx/efflux induces a gradient of current–source density in the surrounding medium. The timedependenceof transmembranepotentialsaremimickedby theLFP(Okunet al.,2009), andlikelybythe macroscale(ECoG)potential as well.  F , The PSD shifts associated with changes in mean firing rate from presynaptic inputs are broadband innature (spread across all frequencies), with a characteristic  P  1/f   form (i.e., the power in the PSD falls off withincreasing frequency according to the exponent,  ). G , The P 1/f  PSD structure might emerge from the combinationsof three simple processes. The first is Poisson-distrib uted input spikes [as in A, reflected in the rate measured by Manninget al. (2009)]. The second is a characteristic postsynaptic current with exponential decay, which produces a 1/f 2 form

followingakink(grayarrow)atafrequencydeterminedbythedecaytimeatthesynapse.ThelastprocesstoshapethePSDis the integration of inward currents over time in the dendrite (as in  D  and   E ). This model demonstrates how therelationship between firing rate and broadband change observed by Manning et al. (2009) might arise. Model adoptedfrom Bedard et al. (2006) and Miller et al. (2009b).

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Miller KJ, Zanos S, Fetz EE, den Nijs M, OjemannJG (2009a) Decoupling the cortical powerspectrum reveals real-time representation of individual finger movements in humans.J Neurosci 29:3132–3137.

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