2015 an in Depth View of Avian Sleep

Neuroscience and Biobehavioral Reviews 50 (2015) 120127

Contents lists available at ScienceDirect

Neuroscience and Biobehavioral Reviews

journa l h om epa ge: www.elsev ier .com/ locate /neubiorev

Review

An in depth view of avian sleep

Gabril Ja Cognitive NeuThe Netherlandb Avian Sleep G

a r t i c l

Article history:Received 19 MReceived in reAccepted 26 JuAvailable onlin

Keywords:SleepSlow wavesBirdMemoryImprintingMultielectrode

Contents

1. Introd2. Delvin3. Recor4. Futur

4.1. 4.2.

5. ConclAcknoAppeRefer

1. Introdu

A growinto mammalinformationet al., 2011Cirelli, 201

Correspon Correspon

E-mail add(N.C. Rattenbo

http://dx.doi.o0149-7634/ uction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120g deep into the sleeping birds brain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121

ding deep brain activity using high-density multielectrodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121e directions: systems-level memory processing in birds? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122Hippocampal memories . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122Imprinting memories . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125

usions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125wledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125

ndix A. Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125ences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125

ction

g body of research on animals ranging from fruit iess to birds suggests that sleep is involved in processing

acquired during wakefulness (Abel et al., 2013; Donlea; Margoliash, 2010; Rasch and Born, 2013; Tononi and4). In mammals, the brain rhythms that occur during

ding author. Tel.: +31 302535412.ding author. Tel.: +49 8157932279.resses: [email protected] (G.J.L. Beckers), [email protected]).

sleep and its sub-states rapid eye movement (REM) and non-REM(NREM) sleep, have been implicated in processing information bothlocally within small neuronal assemblies and across brain regions(e.g. hippocampus and neocortex) at the systems-levels (Huberet al., 2004; Rasch and Born, 2013; Tononi and Cirelli, 2014). How-ever, the exact nature of information processing and the role playedby these rhythms remain actively debated (Frank, 2013; Rasch andBorn, 2013; Tononi and Cirelli, 2012, 2014). Interestingly, despitelacking the laminar neuronal organization found in the neocortex(Medina and Reiner, 2000; Wang et al., 2010), birds exhibit similarsleep states and in many, but importantly not all, respects, simi-lar sleep-related brain activity (Rattenborg et al., 2011). Althougha growing body of research suggests that avian sleep also plays a

rg/10.1016/j.neubiorev.2014.07.0192014 Elsevier Ltd. All rights reserved..L. Beckersa,, Niels C. Rattenborgb,

robiology and Helmholtz Institute, Departments of Psychology and Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht,sroup, Max Planck Institute for Ornithology, Eberhard-Gwinner-Strasse 11, 82319 Seewiesen, Germany

e i n f o

arch 2014vised form 21 July 2014ly 2014e 5 August 2014

a b s t r a c t

Brain rhythms occurring during sleep are implicated in processing information acquired during wakeful-ness, but this phenomenon has almost exclusively been studied in mammals. In this review we discussthe potential value of utilizing birds to elucidate the functions and underlying mechanisms of such brainrhythms. Birds are of particular interest from a comparative perspective because even though neuronsin the avian brain homologous to mammalian neocortical neurons are arranged in a nuclear, rather thana laminar manner, the avian brain generates mammalian-like sleep-states and associated brain rhythms.Nonetheless, until recently, this nuclear organization also posed technical challenges, as the standardsurface EEG recording methods used to study the neocortex provide only a supercial view of the sleep-ing avian brain. The recent development of high-density multielectrode recording methods now providesaccess to sleep-related brain activity occurring deep in the avian brain. Finally, we discuss how intrace-rebral electrical imaging based on this technique can be used to elucidate the systems-level processingof hippocampal-dependent and imprinting memories in birds.

2014 Elsevier Ltd. All rights reserved.

G.J.L. Beckers, N.C. Rattenborg / Neuroscience and Biobehavioral Reviews 50 (2015) 120127 121

role in processing information (Brawn et al., 2010; Dergnaucourtet al., 2005; Gobes et al., 2010; Jackson et al., 2008; Shank andMargoliash, 2009), when compared to mammals, little research hasfocused on the role sleeps sub-states and associated brain rhythmsper se playsystems-levlargely untabrain rhythtargets andstrictly mam

The late bird-based robiologicachicken chiconsolidatioInterestinglinvestigate ing memorneither of uclosely relaIn additionding methothe role sleein birds, inc2012; Beckboth evaluato speculateof sleep and

2. Delving

In mammbe measurecommonly (Massiminithe large elmalian braithe neocortbrain (Fig. rons favors EEG. Speciperpendicuity is synchopen electret al., 2012)descriptionhas led to sewakefulnessystems-levcess informregions (ColSteriade, 20between reand Kleinfe

In contrgous neuromanner (Figaddition, nethe unidirecand Reinerences in neuorchestrateas in mammhigh-ampliRattenborg

during REM sleep (Low et al., 2008; Scriba et al., 2013). Although theneuronal physiology underlying EEG slow-waves has been studiedlittle in birds when compared to mammals, as in mammals, avianslow-waves appear to reect the slow-oscillation (typically

122 G.J.L. Beckers, N.C. Rattenborg / Neuroscience and Biobehavioral Reviews 50 (2015) 120127

Fig. 1. Organi ) reptsubdivisions p dge; Pthe crocodile b

Figure adapted

latency of threcordings,neuronal acimpossible

Becauseand more gral resolutiostudy of sleWe recentlythe zebra potentials (both drawbsuch intracerecordings Consequentnches undnormal slee(Moore et aneuronal osneous NREMslow-wavesgamma (30anesthesia size of the zously with rof brain reg(Fig. 2B). Thoverview o

These rewithin the cess when vand apparethe electrodshort time stions turn owaves are ahas been esin mammalBarth, 201Murphy et et al., 2011nique also pwith traditinside the ba 2-D surfacin the zebra3-D space. Saction potepotential ac

iate ute the faemend us hichics, a) whtrodd timse vipths d wdditbrainocortrainneocts thns ued f

hare

ure d

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evel chesed t

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lonzation of the telencephalon in (A) mammals (rodent), (B) birds (songbird) and (Callidum, striatum, and pallium. Abbreviations: ADVR, anterior dorsal ventricular rirain and is not shown here (cut at stippled line).

from Jarvis (2009) and Jarvis et al. (2013).

is activity was highly variable. In serial single-electrode the spatially distributed nature of such event-relatedtivity would be invisible, and it would be difcult if notto localize such deep-brain activity in EEG recordings.

silicon multielectrodes are able to capture both locallobal aspects of neural activity with very high tempo-n, this technique opens up new opportunities for theep-related neural mechanisms and functions in birds.

started characterizing sleep-related neural activity innch, using 64-electrode recording of unit and local eldBeckers et al., 2014). The small size of zebra nches hasacks and benets. Given the small size of this species,rebral measurements are as yet not feasible for chronic

in freely behaving and spontaneously sleeping animals.ly, as a rst step, we performed acute recordings iner isourane anesthesia, which is known to activatep-promoting regions in the mammalian hypothalamusl., 2012). Moreover, in mammals, anesthetics inducecillations comparable to those occurring during sponta-

sleep (Chauvette et al., 2011; Steriade, 2006); although are more synchronous, down-states are longer, and100 Hz) power is higher under ketamine-xylazine(Chauvette et al., 2011). Finally, a benet of the smallebra nch brain is that it allows us to sample simultane-eadily available multielectrode probes from more typesions than would be possible in a bigger brained birdis is particularly important when trying to get a broadf how the avian brain works as a system during sleep.cordings showed that slow-wave electrical activity

zebra nch brain appears as a globally distributed pro-iewed on longer time scales (i.e. seconds), with similarntly simultaneous oscillatory activity across many ofe sites of the array (Fig. 2D). However, when viewed oncales (i.e. tens of milliseconds), the peaks of the oscilla-ut to be time shifted across the array, showing that slow-

traveling phenomenon in the avian brain (Fig. 2E), as

immedconstitThird, arrangenableplots wdynam(Fig. 2Fto elecing), an1). Thethe dereveale

In aavian the neavian bin the suggesfunctiopresumtraits s

4. Futbirds?

Thethe temlocal lapproaexpandsectionthat wIn addiresolvetablished for slow-waves occurring during NREM sleeps (Chauvette et al., 2011; Hangya et al., 2011; Luczak and2; Massimini et al., 2004; Mohajerani et al., 2013, 2010;al., 2009; Nir et al., 2011; Stroh et al., 2013; Volgushev). Importantly, the intracerebral multielectrode tech-rovided new insights that would not have been gainedional techniques. First, because the array placementrain can be varied, and measurements are not limited toe, as is the case in EEG, we were able to show that waves

nch brain propagate in highly variable directions inecond, in addition to local eld potentials, we recordedntial activity that propagated in concert with local eldtivity, indicating that slow-waves were occurring in the

tilian sleepmammals a

4.1. Hippoc

The follsystems-levOur objectithe evidenc(Tononi anpresent theuated fromfuture reseailes (crocodile). Shown are sagittal views, with color-coding for theDVR, posterior dorsal ventricular ridge. The olfactory bulb is long in

vicinity of the electrode sites (


Fig. 2. High-dshank has 8 elesquare). (B) Lothe hyperpallioverlies and isLocal eld potrate of 14 kHzlevel of multi-grid of electroLFP and AMUAThe propagatielectrode sites

Figure adapted

Accordinrhythms arehippocamp2013). The hippocampnot events EichenbaumMilner, 195suggests thshifts towathe neocortneuroanatoproviding iensity recording of slow-waves in the zebra nch forebrain. (A) The silicon multi-electroctrodes so that a total of 64 recording sites are organized in a regular grid with 200 m intcation of the silicon multi-electrode probe in the hyperpallium inserted sagittally to emphum consists of the hyperpallium apicale (HA), the interstitial part of hyperpallium apicale

interconnected with the mesopallium (M) and nidopallium (N). Recordings were made ential and multi-unit activity (MUA) from a single electrode showing the relationship be, and off-line ltered to obtain local eld potentials (LFP, 0.1350 Hz) and multi-unit actunit action potential ring, the MUA signal is rectied and decimated (AMUA). (D) 5 s epide sites. Oscillations appear to be globally distributed. (E) Detail of the LFP and AMUA p

signals, occurs at slightly different times across the electrode grid, rst at sites in the bong nature of the activity peak is more easily seen when visualized in a sequence of image, and pixel color and gray levels correspond to LFP and AMUA magnitudes.

from Beckers et al. (2014).

g to a prominent model, NREM sleep-related brain thought to orchestrate the systems-level processing ofal-dependent memories in mammals (Rasch and Born,model stems from the observation that damage to theus in humans causes amnesia for recent events, butthat occurred in the distant past (Bayley et al., 2006;, 2000; Frankland and Bontempi, 2005; Scoville and

7; Smith and Squire, 2009; Teng and Squire, 1999). Thisat recall of initially hippocampal-dependent memoriesrd depending less on the hippocampus and more onex over time. This observation and the connectionalmy of the hippocampus and temporal lobe structurest with input led to the idea that during wakefulness

the hippocain from virMcClellandinput to qutributing toor exposurthe entire ecoordinatedneocortex irepresentatting informsuggested ttex, but ratde probe consists of 8 shanks that are inserted into brain tissue. Eacher-site spacing that extends over a 1400 m 1400 m plane (yellowasize the coverage of the brain possible with readily available probes:

(IHA), and the hyperpallium densocellulare (HD). The hyperpalliumin this plane and horizontally in the same region as shown in (D). (C)tween the two. Electrical potentials were recorded with a sampling

ion potentials (0.55 kHz). To obtain a signal that corresponds to thesode showing the temporal pattern of LFP and AMUA across the 8 8eak indicated with two asterisks in (D). The peak of activity, both inttom right corner and then later at sites in the top half of the grid. (F)

plots. Each image has 8 8 pixels corresponding to the 8 8 grid of

mpus serves as a convergence zone for input funnelingtually the entire neocortex (Eichenbaum, 2000, 2004;

et al., 1995). The hippocampus is thought to use thisickly form an index of the neocortical circuits con-

a certain event in a manner such that the recall of,e to, portions of an experience can elicit the recall ofxperience (i.e. an episodic memory). During sleep, the

replay of past experiences in the hippocampus ands thought to lead to the strengthening of the neocorticalion of the memory and its integration within preexis-ation stored in the neocortex. More recently, it has beenhat the entire memory is not transferred to the neocor-her its episodic component remains dependent on the


Box 1: Evolution of sleep in mammals and birdsThe presence of similar sleep states in mammals and birdseither retheir shagent evoand REMassessmtiles [Notype of rmammalilar sleepis rife wiity includbehaviorbut not slamplitudcases, w2007). Ment reseaConsequods seemexact difflikely incAmong tplay an imreportedthin threeplacemenin birds, mneocortethe dorsthat elecstudies, eactivity psleep-reling strucdescribedlong festover, by Sauropsibehave astanding

hippocampa more genand DurranMoscovitch

Althougremains dehave been ipocampus i(sharp-wavsharp-wavecal neuronsreplay this2010; Ji anSWR complcal membraof the slowlamocorticarhythms (Steriade, 2to the strenory being Sirota et aldinated rephippocamp

direct projections from the hippocampus to the medial prefrontalcortex (mPFC) (Jay and Witter, 1991; Swanson, 1981; Thierry et al.,2000) and from the mPFC to regions providing input to the hip-

pus, as well as several other lines of evidence suggest that theplaysenanGais and Bhe eted inrn, 2

pite sometal drocesNotaed in

det011)ensean hich r

ing iceivthe hceivean ects the inheritance of comparable sleep states fromred (stem amniote) ancestor, or a process of conver-lution. Our understanding of the evolution of NREM

sleep in mammals and birds depends on an accurateent of sleep-related brain activity in non-avian rep-te: as members of the taxon Dinosauria, birds are aeptile]. Unfortunately, in contrast to the situation ins and birds wherein most studies report largely sim--related EEG activity, the non-avian reptile literatureth unresolved controversies. Reports of brain activ-e mammalian/avian-like slow-waves occurring duringal sleep, slow-waves occurring during wakefulness,eep, and intermittent sharp-waves arising from a low-e background EEG pattern during sleep and, in someakefulness (reviewed in Hartse, 1994; Rattenborg,any of the discrepancies are found between differ-rch groups, even when working on the same species.ently, the lab-specic recording conditions and meth-

to contribute to the variation in reports; although theerences between labs remain poorly understood andlude several factors.he potential explanations, electrode placement mayportant role. In most cases, the EEG electrodes were

ly placed on the dura overlying the dorsal cortex, a-layered neocortex-like structure. However, the exactt was only carefully described in a few studies, and asost of the neurons thought to be homologous to the

pocammPFC (Bench2004; Mlle Peyracreviewand Bo2011).

Desalbeit damenand psleep. reportreadilyet al., 2some sthe avipus whfunnelonly rebrain: only reShanahx are arranged in large nuclear structures well below

al cortex (Fig. 1C). Consequently, it is conceivabletrode placement contributed to the variation acrossspecially if different brain structures exhibit differentatterns during sleep. The simultaneous recording ofated brain activity in the dorsal cortex and underly-tures using the high-density depth recording methods

herein may serve as a powerful tool for resolving thisering problem in comparative sleep research. More-using this approach to compare how the brains ofds (i.e. avian and non-avian reptiles) and mammalss systems during sleep, we may gain greater under-

of the evolution of systems-level memory processing.

us, whereas other components become represented ineral manner as part of schemas in the neocortex (Lewist, 2011; Preston and Eichenbaum, 2013; Winocur and, 2011).h the exact nature of such systems-level processingbated, the brain rhythms occurring during NREM sleepmplicated in this process. During NREM sleep the hip-ntermittently generates synchronous bursts of activityes) followed by high-frequency ripples. During such

ripple (SWR) complexes, hippocampal and neocorti- that red in a particular sequence during wakefulness

sequence in a coordinated manner (Benchenane et al.,d Wilson, 2007; Peyrache et al., 2009). The timing ofexes is inuenced by the slow-oscillation of neocorti-ne potentials such that they occur during the up-state-oscillation when neocortical neurons are active. Tha-l spindles intermittent waxing and waning 1215 Hzalso occur during the up-state of the slow-oscillation006) and are thought to produce conditions conducivegthening of the neocortical representation of the mem-replayed (Isomura et al., 2006; Mlle et al., 2009;., 2003; Wierzynski et al., 2009). Over time this coor-lay is thought to lead to reduced involvement of theus in the recall of memories. Finally, the presence of

regions in t the functdirect inpupus (Atoji aet al., 2013)lium densoto the hippupon the Hof projectio1999), or oseemingly informationmammalianthe avian hpocampus iepisodic mhippocampinformationof episodicdepend on tures (Rattecontrast tomemories dependent described ilectively, thprovide comlacking the hippocampin the syste

Althouggests that hippocampless play aThis could which the nisms/rhythplay a role a key role in orchestrating or overseeing this processe et al., 2010; Bontempi et al., 1999; Frankland et al.,et al., 2007; Mander et al., 2013; Maviel et al., 2004;orn, 2009; Paz et al., 2007, 2009; Pelletier et al., 2004;

al., 2009; Restivo et al., 2009; Takashima et al., 2006; Colgin, 2011; Frankland and Bontempi, 2005; Huber014; Preston and Eichenbaum, 2013; Rattenborg et al.,

exhibiting mammalian-like NREM sleep, the available,times limited, evidence suggests that there are fun-ifferences between how mammals and birds forms hippocampal memories during wakefulness andbly, SWRs and thalamocortical spindles have not been

birds, despite numerous studies using methods thatect such events in mammals (reviewed in Rattenborg. This apparent difference in neurophysiology may make

when one compares the nature of information reachingippocampus. In contrast to the mammalian hippocam-eceives highly processed high-order multimodal inputn from most of the neocortex, the avian hippocampuses information from a relatively small portion of theippocampus and regions providing it with direct input

olfactory and visual information (Atoji and Wild, 2006;et al., 2013). Moreover, most high-order associationhe DVR, including the nidopallium caudolateral (NCL)ional analog of the mammalian PFC do not providet to or receive direct output from the avian hippocam-nd Wild, 2006; Krner and Gntrkn, 1999; Shanahan. The NCL does receive direct projections from hyperpal-cellulare (HD), which in turn is reciprocally connectedocampus, but the NCL does not appear to project backD (Krner and Gntrkn, 1999). The apparent absencens from the NCL to the HD (Krner and Gntrkn,ther regions providing the hippocampus with input,precludes a role for the NCL in inuencing the ow of

into and out of the hippocampus, as suggested for the PFC. Furthermore, as suggested by the limited input to

ippocampus, in contrast to mammals wherein the hip-s thought to function as a convergence node for formingemories of what happened where and when, the avianus seems to be involved primarily in processing spatial

(Coppola et al., 2014). As such, behaviors suggestive-like memory in birds (Salwiczek et al., 2010) mayboth hippocampal and extra-hippocampal brain struc-nborg and Martinez-Gonzalez, 2011, 2013). Finally, in

mammals, there is no solid evidence for the recall ofinitially dependent upon the hippocampus becomingupon extra-hippocampal brain regions over time, asn mammals (reviewed in Rattenborg et al., 2011). Col-ese apparent differences between mammals and birdsparative support to the model proposed in mammals;

mammalian-like ow of information into and out of theus, birds may have no need for the rhythms implicatedms-level processing of this information.h this comparison between mammals and birds sug-there are differences at the systems-level in howal information is processed, avian sleep may nonethe-

role in the systems-level processing of information.occur within the comparatively limited system withinhippocampus functions, perhaps via different mecha-ms from those described in mammals. Sleep may also

in the systems-level processing of memories that do


not involve the hippocampus, including song learning (reviewedin Rattenborg et al., 2011). In either case, the high-density depthrecording methods described herein may be used to identify can-didate regions and rhythms involved in such processes throughrevealing co

4.2. Imprin

Imprintias chickensally their pathe mechaninvestigatedprocessing rst few hodepends onever, Hornlonger depememory haunknown, rHoney et al

Sleep maory trace inIn a semin2008), Hornto an impriimprinting two experimimprinting undisturbeda 1.5 h testireducing thwere disturturbed durito the impriboth groupsmore IMM during the rst and alloin its sub-stpower (perhduring the than in thethat sleep pimprinting of this papechanges in specic mein the systeby Horns ealready com

Further iries in the IMprocessing high-densitcally, regionsleep, particprocessing be prime caof imprintindination aninto generasystems-leveven informhippocamp

5. Conclusions

The development of high-density recording methods serves asa powerful tool for exploring the depths of the avian brain. This

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ting memories

ng, the tendency for newly hatched precocial birds, such, to rapidly form memories of large moving objects (usu-rents) has served as a powerful model for investigatingisms involved in memory consolidation. As extensively

by Horn and colleagues, visual imprinting involvesat both the local and systems-level. Initially, for theurs after imprinting, recall of the imprinting stimulus

the intermediate and medial mesopallium (IMM). How-s lesion studies have shown that after 46 h recall nonds solely upon this brain region, suggesting that thes been processed at a systems-level and other, as yetegions can support its recall (Cipolla-Neto et al., 1982;., 1995).y play a role in both the initial processing of the mem-

the IMM and its subsequent systems-level processing.al paper published in Current Biology (Jackson et al.,

and colleagues showed that sleep following exposurenting stimulus is important for the initial processing ofmemories. In this study, the chicks were divided intoental groups immediately following exposure to the

stimulus. Chicks in one group were allowed to sleep during a 6 h post-training session, and then, following

ng period, were disturbed for the next 6 h, presumablyeir time spent sleeping. In the second group, the chicksbed for the rst 6 h and then allowed to sleep undis-ng the last 6 h. The number of IMM neurons respondingnting stimulus was assessed at the end of each session in. Importantly, in chicks that were allowed to sleep rst,neurons were responsive to the imprinting stimulusnal testing period, than in chicks that were disturbedwed to sleep second. Although sleep and the time spentates were not quantied directly, the amount of 56 Hzaps occurring during NREM sleep) recorded in the IMM

rst session was greater in the group left undisturbed disturbed group. Collectively, these ndings indicatelays an important role in the initial consolidation of

memories in the IMM. More generally, a major strengthr was that the authors were able to track sleep-relatedthe behavior of individual neurons contributing to amory. Understandably, the potential role sleep playsms-level processing of imprinting memories revealedarlier IMM lesion studies was beyond the scope of thisprehensive initial study.nsight into sleeps role in processing imprinting memo-M, and its potential involvement in the systems-level

of such information may be gained through using they depth recording methods described herein. Speci-s exhibiting coordinated activity with the IMM duringularly during the time interval when the systems-levelof the imprinting stimulus is thought to occur, wouldndidates for extra-IMM regions supporting the recallg memories. More generally, the nature of the coor-

d the rhythms employed might provide further insightl principles that brains use to process information at ael. In this respect, this extension of Horns work might

our understanding of the systems-level processing ofal memories in mammals, including ourselves.

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Dergnaaffecs already revealed a complex storm of activity occur-elatively local (1.4 mm 1.4 mm) scale. By scaling upch, we hope to gain a greater understanding of howrain works as a system of systems to process infor-ing sleep. Comparing these ndings in birds to thoseom mammals and relating the results of such compar-ilarities and differences in neuroanatomy, may revealrinciples of heuristic value for understanding the mam-n that might otherwise remain obscure using a strictly-based investigative approach. The extensive ground-

y Horn and his colleagues serves as a powerful system inply this comparative approach to understanding sleep.

gements

rk was supported by the Max Planck Society and bym the People Programme (Marie Curie Actions) ofn Unions Seventh Framework Programme (FP7/2007-r REA grant agreement n 302549.

. Supplementary data

entary material related to this article can be found,ine version, at http://dx.doi.org/10.1016/j.neubiorev.9.

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An in depth view of avian sleep1 Introduction2 Delving deep into the sleeping bird's brain3 Recording deep brain activity using high-density multielectrodes4 Future directions: systems-level memory processing in birds?4.1 Hippocampal memories4.2 Imprinting memories

5 ConclusionsAcknowledgementsAppendix A Supplementary dataReferences

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2015 an in Depth View of Avian Sleep