Behavioural Brain Research 222 (2011) 236245

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Behavioural Brain Research

journal homepage: www.elsevier.com/locate/bbr

Review

A bird-brain view of episodic memory

N.C. Rattenborg , D. Martinez-Gonzalez
Max Planck Institute for Ornithology Seewiesen, Sleep and Flight Group, Eberhard-Gwinner-Strasse, 82319 Seewiesen, Germany

a r t i c l e i n f o a b s t r a c t

Article history: In humans, the hippocampus plays a critical role in the formation of episodic memories. Although non-
Received 28 February 2011 human animals are unable to report whether they also re-experience past events, at least some birds
Accepted 11 March 2011 and mammals exhibit episodic-like memory characterized by an ability to recall what happened where
Available online 21 March 2011
and when. In mammals, the hippocampus interacts closely with virtually the entire neocortex to form
episodic-like memories. The hippocampus receives highly processed information from high-order asso-
Keywords:
ciation areas, and thereby the rest of the neocortex. Distinct neurophysiological hippocampal rhythms
Dorsal ventricular ridge
(theta and sharp-wave ripples) coordinate activity between the hippocampus and high-order associ-
Nidopallium
Mesopallium
ation areas during the encoding and retrieval of information contributing to episodic-like memories.
Prefrontal cortex Although recent studies have demonstrated that food hoarding birds are able to remember what food
Sleep they hid where and when, neuroanatomical and neurophysiological studies suggest that there may be a
fundamental difference between episodic-like memory in birds and mammals. In contrast to the mam-
malian hippocampus, the avian hippocampus only receives visual and olfactory input; most high-order
association areas in the avian brain involved in performing functions similar to those performed by neo-
cortical association areas do not project to the hippocampus or structures providing it with direct input.
Consistent with this neuroanatomical difference, mammalian-like rhythms involved in communicating
between the hippocampus and neocortical high-order association areas have not been found in birds.
Collectively, this suggests that information contributing to episodic-like memory is more limited and
processed in a different manner in birds when compared to mammals.
2011 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 236
2. Neural substrates of episodic-like memory in mammals and birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237
2.1. Mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237
2.1.1. Neuroanatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237
2.1.2. Neurophysiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237
2.2. Birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239
2.2.1. Neuroanatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239
2.2.2. Neurophysiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241
3. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 242
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 242
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 242

1. Introduction hoarding birds [2]. During the last 12 years, a growing body of work
has shown that food hoarding birds, such as Western scrub-jays
The human capacity to recall specic personal events from the (Aphelocoma coerulescens), black-billed magpies (Pica pica), and
past is referred to as episodic memory [1]. A recent special issue black-capped chickadees (Poecile atricapillus), are able to remem-
in Behavioural Brain Research highlighted advances in research ber what food they hid where and when [28]. These essential
on episodic memory, including seminal work on memory in food components of episodic memory are stored in an integrated man-
ner, such that retrieval of one component automatically activates
the other components, and thereby possibly the entire memory
Corresponding author. Tel.: +49 8157 932 279; fax: +49 8157 932 344. of a specic event [911]. This integrated form of what, where,
E-mail address: rattenborg@orn.mpg.de (N.C. Rattenborg). when memory is typically referred to as episodic-like memory in

0166-4328/$ see front matter 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.bbr.2011.03.030
 N.C. Rattenborg, D. Martinez-Gonzalez / Behavioural Brain Research 222 (2011) 236245
non-human animals that cannot verbally report whether they re-
experienced the past event [6,7]. Although it is unknown whether
birds experience episodic memories like those experienced by
humans [1], the nding that jays plan for future needs [12] suggests
that they have some capacity for mental time travel ([13], but see
[14]), and therefore might use similar cognitive processes to travel
mentally back in time when retrieving hidden food.
The evidence for episodic-like memory in food hoarding birds is
compelling. However, little is known about how the avian brain
processes such memories. In this review, we examine whether
birds and mammals use similar brain areas and processes to gener-
ate episodic-like memories. Although extensive evidence indicates
that the avian hippocampus is involved in processing and storing
spatial information contributing to episodic-like memory [1517],
the potential role of interactions between the hippocampus and
high-order association areas has been largely overlooked. Conse-
quently, we focus on this aspect of episodic-like memory.
Mammals and birds independently evolved large brains [18,19]
capable of performing complex cognitive processes [2023]. In both
groups, encephalization was due primarily to expansion of the pal-
lium, the dorsal part of the neural tube. However, the resulting
pallial organization differs markedly between mammals and birds.
The majority of the mammalian pallium consists of the laminar neo-
cortex, whereas in birds it is organized mainly as nuclear structures
[21,24]. Although recent studies have emphasized the convergent
aspects of cognition, divergence in pallial organization and related
neurophysiology suggest that there may be a fundamental differ-
ence between how pallial structures in mammals and birds process
information [25]. Notably, whereas the mammalian hippocampus
interacts with virtually the entire neocortex, the available evidence
suggests that interactions between the avian hippocampus and pal-
lium are more limited, a difference in brain organization that may
have implications for our understanding of episodic-like memory
in birds.
2. Neural substrates of episodic-like memory in mammals
and birds
2.1. Mammals
2.1.1. Neuroanatomy
In humans, the formation of episodic memories for specic
personal events depends on the hippocampus [1]. Patients with
lesions restricted to the hippocampus are unable to form new
episodic memories of recently experienced events, or to recall
events occurring shortly before the damage [2632]. The hip-
pocampus also appears to be necessary for episodic-like memory
in non-human mammals [7,33]. The mammalian hippocampus is
connected to the neocortex in a manner that makes it ideally
suited for forming episodic memories derived from information
processed throughout the neocortex [34,35]. Information destined
for the hippocampus is conveyed via parallel sensory pathways and
then converging associational pathways. Specically, information
passes rst through primary and then secondary sensory cortices,
association cortices, multimodal association cortices, and then the
parahippocampal and perirhinal cortices, and nally the entorhi-
nal cortex before entering the hippocampus (Fig. 1) [34,35]. As
information ows from primary sensory areas to the hippocam-
pus it is processed at each step, becoming more associative in
nature. Notably, rather than simply serving as a relay for infor-
mation to the hippocampus, the parahippocampal, perirhinal, and
entorhinal cortices are also involved in forming high-order asso-
ciations contributing to episodic-like memories [32,36,37]. The
prefrontal cortex (PFC) also inuences information entering the
hippocampus via its reciprocal connections with the parahip-
237
Neocorcal Associaon Areas
PFC
(Dorsal Pallium)
Perirhinal Parahippocampal
Cortex Cortex
Entorhinal
Cortex
Piriform
Hippocampus
Cortex
Fig. 1. Extensive connections between the mammalian hippocampus and neocorti-
cal association areas. Virtually all association areas in the neocortex (dorsal pallium)
are reciprocally connected to the hippocampus via the parahippocampal, perirhi-
nal, and entorhinal cortices. The prefrontal cortex (PFC) is thought to inuence the
ow of information to and from the hippocampus via reciprocal connections to
each of these regions. The hippocampus communicates with association regions,
and thereby the rest of the neocortex, via the entorhinal, parahippocampal, and
perirhinal cortices. The hippocampus also provides direct input to the PFC.
pocampal, perirhinal, and entorhinal cortices [27,35,38]. As a result,
rather than receiving direct sensory information related to an event,
the hippocampus receives highly processed multimodal associa-
tive information derived from virtually every neocortical area
[27,39,40]. In conjunction with this hierarchical organization, the
internal circuitry and cellular physiology of the hippocampal sub-
regions, the dentate gyrus, CA1 and CA3, are thought to instill the
hippocampus with the capacity to rapidly encode [4143] unique
but similar events (pattern separation), and to reconstruct entire
episodes in response to activation of a small subset of neurons
involved in the memory (pattern completion), requisites for the
formation and recall of episodic memories [44]. Finally, during
recall of an episode, the hippocampus is thought to re-instantiate
the experience via reciprocal connections to the entorhinal cortex,
and thereby neocortical areas initially involved in processing the
experience.
2.1.2. Neurophysiology
Brain rhythms are fundamental mechanisms through which the
brain coordinates information processing between areas [45,46].
During memory encoding and recall, the mammalian hippocam-
pus communicates with the neocortex via two mechanistically
linked reciprocal modes of activity, the theta (612 Hz) rhythm
and sharp-wave ripples (SWRs) [47,48]. The hippocampal theta
rhythm occurs during translational movement in awake animals
and during rapid-eye movement (REM) sleep [49,50]. Projections
from theta pacemaker cells in the medial septum to the hippocam-
pus play an important role in the genesis of the hippocampal theta
rhythm [50,51]. In rats, lesions to the medial septum that disrupt
the hippocampal theta rhythm also disrupt the formation of spa-
tial memories [5254]. During encoding, the theta rhythm may
contribute to episodic memories by providing spatial context and
temporal order to memories [5557], although the exact mecha-
nism remains debated (reviewed in [55]). The encoding and retrieval
of memories as an animal moves through the environment may
occur at different phases of the theta rhythm [58], in conjunction
with theta-phase synchronized gamma (30150 Hz) oscillations
[5964]. The theta rhythm may also facilitate recall by synchroniz-
ing activity between the hippocampus, entorhinal cortex, and other
238 N.C. Rattenborg, D. Martinez-Gonzalez / Behavioural Brain Research 222 (2011) 236245

brains areas (reviewed in [55]). Of particular interest, the hippocam-
pal theta rhythm synchronizes activity in the medial PFC (mPFC)
[6572], apparently via direct excitatory projections from CA1
hippocampal neurons to the mPFC [7375]. Consistent with its pro-
posed executive role in retrieving context-relevant memories from
long-term memory in the rest of the neocortex [76], the PFC may
use information received directly from the hippocampus to mon-
itor and lter information entering and leaving the hippocampus
during exploration via its reciprocal connections to the parahip-
pocampal, perirhinal, and entorhinal cortices [35,38,7779]. Lesion
studies also suggest that the mPFC contributes to retrieving specic
components of episodic-like memories [33,80]. Finally, the theta
rhythm occurring during REM sleep has also been implicated in
processing hippocampal memories [81], perhaps by synchronizing
activity between the hippocampus and mPFC [70] and other areas
such as the basolateral amygdala [82].
In addition to the theta rhythm, the mammalian hippocampus
generates SWRs, intermittent highly synchronous bursts of activity
in CA3 neurons that cause high-amplitude (e.g. 2 mV), sharp-wave
eld potentials in the dendritic layer and 100200 Hz ripples in
the pyramidal layer of CA1 [50,83,84]. SWRs occur during pauses
in translational movements, feeding, grooming, quiet wakefulness,
and most frequently during slow-wave sleep (SWS). Functional the-
ories for SWRs stem from their temporal relationship to the activity
of place cells, hippocampal neurons that re when an animal is in
a particular location [85]. As rats move through their environment,
place cells re as the animal traverses the place eld of each cell.
Although much work has focused on the spatial properties of place
cells, they also appear to encode other aspects of an experience
contributing to episodic-like memories [27,8690]. Sequences of
place cell ring that occur as an animal moves through its envi-
ronment are replayed during SWRs occurring during brief pauses
in behavior, quiet wakefulness, and SWS [9195]. Replay during
wakefulness can occur in a forward or reverse order (reviewed in
[91]), whereas that occurring during SWS-related SWRs occurs only
in a forward order [96]. Replay during pauses in waking behav-
ior may be involved in the early stages of processing hippocampal
information, or in the retrieval of information to guide future
behavior [91]. During SWS, replay occurs in a coordinated man-
ner with replay in the neocortex [9799], a phenomenon that may
be involved in integrating new hippocampal memories into pre-
existing neocortical networks [47,100104]. Several recent studies
suggest that the PFC may play a special role in this process [105].
During SWS, SWR-related reactivation occurs 3060 ms prior to
reactivation of associated neural activity in the mPFC [65,98,106].
The hippocampus may drive activity in the PFC via the direct excita-
tory pathway from CA1 neurons to the mPFC [7375]. Coordinated
SWS-related reactivation may be involved in a systems level mem-
ory consolidation process that results in the recall of memories
initially encoded in the hippocampus becoming progressively less

Fig. 2. The pallium in representative species of different vertebrates. Schematic diagrams of frontal sections through the telencephalon of representative species of different
vertebrates (a mouse, a pigeon, the lizard Psammodromus, and the frog Xenopus) showing the pallium colored in grey. In the mouse and most mammals, the most representative
pallial structure is the neocortex (a dorsal pallial derivative), whereas in birds and lizards and other non-avian reptiles it is the dorsal ventricular ridge (DVR, a derivative
of the lateral/ventral pallium). Abbreviations: ACo, anterior cortical amygdalar area; Ap, pallial amygdala (frog); BC, basal amygdalar complex; BST, bed nucleus of the stria
terminalis; cc, corpus callosum; Ce, central amygdala; CPu, caudoputamen (dorsal striatum); DC, lizard dorsal cortex; DP, dorsal pallium; DVR, dorsal ventricular ridge; ec,
external capsule; En, endopiriform nucleus; H, avian hyperpallium; HF, hippocampal formation; Hyp, hypothalamus; ic, internal capsule; GP, globus pallidus; LC, lizard lateral
cortex (olfactory cortex); LGE, lateral ganglionic eminence; LP, lateral pallium; LSt, avian lateral striatum; M, avian mesopallium (dorsal part of the DVR); MC, lizard medial
cortex; MGE, medial ganglionic eminence; MP, medial pallium; MSt, avian medial striatum; N, avian nidopallium (ventral part of the DVR); NCx, neocortex; P, pallium; Pa,
pallidum; Pir, piriform (or olfactory) cortex; rf, rhinal ssure; S, subpallium; SAT, lizard striatoamygdaloid transition area; Se, septum; St, striatum; Th, thalamus (dorsal
thalamus); va, vallecula; VP, ventral pallium; VPa, ventral pallidum. Modied with permission from [23].
 N.C. Rattenborg, D. Martinez-Gonzalez / Behavioural Brain Research 222 (2011) 236245 239

Fig. 3. (A, B) Histological comparison of the hippocampal formation between the rat and pigeon. (A) Layers of the dentate gyrus (DG) and cornu ammonis (CA) are conspicuous
in the rat. (B) The V-shaped layer is the only readily apparent structure in the pigeon hippocampus (Hp). APH: parahippocampal area. (C, D) Location and extent of the pigeon
hippocampal formation (HF, dark grey) and dorsolateral corticoid area (CDL, light grey). (C) Dorsal view. (D) Transverse section. Scale bars in A, B = 1 mm. Reproduced with
permission from [126].

dependent on this structure and more dependent on the PFC over
time [38,105,107116].
In summary, the formation and recall of mammalian episodic-
like memories depends on a hippocampus that receives highly
processed associational information originating from virtually the
entire neocortex. The hippocampus uses distinct neurophysiolog-
ical rhythms to coordinate activity between the hippocampus and
neocortical areas during encoding and retrieval of information con-
tributing to episodic-like memories. In particular, several lines of
evidence suggest that direct connections from the hippocampus to
the PFC play an important role in these processes.
hippocampal formation was dened as a V-shaped medial area (i.e.,
the hippocampus) and the parahippocampal area (APH), a poorly
delineated, thin structure overlying the dorsal portion of the lat-
eral ventricle (Fig. 3). In this review, we follow Atoji and Wild [125]
and dene the avian hippocampus as the pallial area medial to the
paraventricular sulcus (Fig. 4). This area encompasses the medial
portion of the APH and the hippocampus according to Karten and

2.2. Birds

2.2.1. Neuroanatomy
The pallium enlarged in mammals and birds, however, the
organization of the avian pallium more closely resembles that of
their reptilian relatives than that of their more distant mammalian
relatives (Fig. 2). Comparisons of pallial areas in vertebrates are
most readily discussed within the context of recent developmental
gene expression studies. During development, four pallial sectors
(medial, dorsal, lateral, and ventral) can be identied [23,117121].
The medial sector becomes the hippocampus in mammals and
birds, and the medial cortex in reptiles, structures implicated Fig. 4. Hypothesized homology of hippocampal formation subregions between
in processing and storing spatial information [1517,122,123]. mammals and birds [126]. The medioventral V-shaped layer (shaded light grey) is
Despite this functional similarity, differences in cytoarchitecture, comparable to the mammalian dentate gyrus, the dorsomedial region (DM) to cornu
neurochemistry, and connectivity have complicated attempts to ammonis (CA) and the subiculum, and the dorsolateral region (DL) to the entorhinal
cortex. Alternative interpretations include the V-shaped layer as the CA and portions
dene the boarders of the avian hippocampus and possible homo-
of DM as the dentate gyrus [127]. Other histologically identied regions include the
logues of the mammalian entorhinal cortex, CA1, CA3, and dentate magnocellular region (Ma), the parvocellular region (Pa), and the cell-poor region
gyrus. Historically, according to Karten and Hodos [124], the avian (Po). CDL: dorsolateral corticoid area. Reproduced with permission from [126].
240 N.C. Rattenborg, D. Martinez-Gonzalez / Behavioural Brain Research 222 (2011) 236245
Hodos [124], and includes commonly proposed homologues of the
mammalian CA areas and the dentate gyrus (reviewed in [125,126],
see also [120,127]). Lateral to the paraventricular sulcus is the dor-
solateral area of the hippocampal formation (DL, part of the former
APH), an area that like the mammalian entorhinal cortex serves
as the main source of input to the hippocampus [125]. Laterally,
DL grades into the dorsolateral corticoid area (CDL), which in turn
joins the piriform cortex ventrolaterally. Like the DL, the CDL also
appears to transmit information to the hippocampus. Although
the DL and CDL have some connectional properties similar to the
entorhinal cortex, recent developmental studies suggest that the
area typically identied as the posterior piriform cortex [124] may
be the avian entorhinal cortex [117,120]. Although several ques-
tions about homology remain unresolved, the conclusions drawn in
this paper do not hinge on one particular interpretation, but rather
apply to all proposals.
The dorsal pallium develops into the neocortex in mammals, the
hyperpallium in birds, and the dorsal cortex in reptiles (Fig. 2). The
neocortex receives visual and somatosensory input from the lem-
nothalamic nuclei of the dorsal thalamus, and visual and auditory
input from the collothalamic nuclei [128130], whereas in saurop-
sids (birds and non-avian reptiles) the dorsal pallium receives
lemnothalamic visual and somatosensory input, but apparently no
direct collothalamic input [131]. The neocortex encompasses the
largest proportion of the pallium in mammals, and, unlike the dor-
sal pallium of sauropsids, includes large multimodal association
areas [35,129].
The lateral and ventral pallia give rise to the claustrum and
pallial portions of the amygdala in mammals, and the dorsal
ventricular ridge (DVR) in sauropsids, a largely nuclear struc-
ture that bulges into the lateral ventricle (Fig. 2). In birds, the
DVR is particularly large (virtually occluding the lateral ventri-
cle) and more differentiated than the DVR in non-avian reptiles,
including crocodilians, the closest living relatives to birds [120].
Although developmental data indicate that the DVR is homolo-
gous as a eld with the mammalian claustrum and pallial amygdala
[119,132,133], collothalamic visual and auditory input to the DVR
is similar to that reaching the extrastriate and auditory neocortex,
respectively [21,131,134,135]. This has led to the suggestion that
certain cell groups in the DVR are homologous to certain layers of
the lateral (extrastriate and auditory) neocortex, rather than the
claustroamygdalar complex [21,134]. Others have suggested that
the DVR is a combination of both the lateral neocortex and claus-
troamygdalar complex as a developmental eld [136]. Reconciling
these different lines of evidence remains a challenge for the eld of
comparative neuroanatomy [137139].
In contrast to the mammalian derivatives of the lateral and
ventral pallia, the DVR encompasses the largest proportion of the
pallium in sauropsids. In amphibians, the out-group to amniotes
(mammals and sauropsids), the dorsal and lateral/ventral pallial
sectors are relatively undeveloped when compared to those in
mammals and sauropsids, respectively (Fig. 2) [140]. Assuming that
the amphibian condition reects the ancestral state of the amniote
pallium, the main difference between the brains of mammals and
sauropsids rests in the pallial sector that underwent the great-
est development: mammals expanded the dorsal pallium, whereas
sauropsids, birds in particular, expanded the lateral and ventral
pallia.
Expansion of the respective pallial structures in mammals and
birds seems to be linked to a subventricular zone (SVZ) of neuronal
proliferation in the developing pallia of each group. A similar SVZ
has not been found in the pallium of amphibians and non-avian
reptiles, including crocodiles, suggesting that this source of neu-
ronal proliferation evolved independently in mammals and birds
[141], and therefore may contribute to encephalization in these
groups. In mammals, a SVZ in the dorsal pallium appears to be
the source of excitatory projection neurons, including associational
neurons in the supragranular layers of the neocortex [142], layers
not found in the three-layered dorsal cortex of non-avian reptiles
[135,143]. Recent evidence suggests that a SVZ in the dorsal pallium
of birds also contributes to the expansion of the hyperpallium [144],
and perhaps the convergent evolution of mammal-like neuronal
types found in this structure, but not the dorsal cortex of non-avian
reptiles [129,143,145]. In addition to the dorsal SVZ, birds have a
more prominent SVZ running along the lateral ventricle that con-
tributes neurons to the DVR, the largest pallial structure in birds
[141,144,146,147].
The avian DVR is involved in forming high-order associations
similar to those performed by association areas in the neocor-
tex. The mesopallium is involved in various types of learning,
including, imprinting [148], song learning [149], avoidance learning
[150], tool manufacture and use [151], and innovative and ex-
ible behaviors in general [152,153]. The nidopallium, the other
major division of the DVR, also appears to be involved in forming
high-order associations [154]. Notably, the nidopallium caudolat-
eral (NCL) shares several features in common with the mammalian
PFC [22,155], despite developing from a different pallial sector.
The NCL is a high-order multimodal association area reciprocally
connected to secondary sensory areas for processing visual, audi-
tory, somatosensory and trigeminal information [156159]. The
NCL is also reciprocally connected to other multimodal association
areas in the nidopallium and mesopallium [157,159]. In addi-
tion to processing multimodal sensory information, the NCL also
appears to be involved in working memory and executive con-
trol, high-order cognitive functions similar to those performed by
the PFC [155,160162]. In both the PFC and NCL, working mem-
ory is dependent upon the release of dopamine from projections
from the midbrain ventral tegmental area and the substantia nigra
[155,163166]. Collectively, the available evidence suggests that
the mammalian PFC and avian NCL perform similar functions.
Moreover, in general, complex cognition in birds seems to depend
on the DVR, a lateral and ventral pallial derivative, rather than the
dorsal pallium, as in mammals.
Despite comprising high-order association areas involved in
complex cognitive processes similar to those performed by
association areas in the neocortex, unlike the neocortex, the
DVR shares few connections with the hippocampus (Fig. 5)
[125,127,157,158,167,168]. Moreover, although it remains unclear
which brain area is homologous to the mammalian entorhinal
cortex the main structure through which information reaches
the mammalian hippocampus candidate entorhinal-like areas
providing input to the avian hippocampus, such as the CDL,
APH, DL, or entorhinal cortex, as dened by Puelles et al. [120],
also do not appear to receive projections from most of the DVR
[125,157,158,167169]. Only the frontolateral nidopallium, an area
of the DVR involved in processing high-order visual informa-
tion [170] and the caudoventral nidopallium (NCV), apparently
a part of the limbic system [171], project to the hippocam-
pus via the APH and CDL, respectively [125,157,158,167,168].
Although not originating in the DVR, the only other sensory modal-
ity that provides input to the hippocampus is olfaction [125].
Olfactory input from the piriform cortex reaches the hippocam-
pus directly and indirectly via the CDL, DL, and densocellular
part of the hyperpallium [125,129,172,173]. Finally, in contrast
to the mammalian PFC, the avian PFC (NCL) does not receive
direct projections from the hippocampus or candidate entorhinal-
like areas [125,157,158,167,174]. Consequently, in contrast to the
mammalian hippocampus, which receives input from virtually all
high-order association areas, and thereby the rest of the neocor-
tex, connections between the avian hippocampus and major pallial
association areas in the DVR are limited [34,175]. As expected given
their close relationship to birds, few connections have also been
 N.C. Rattenborg, D. Martinez-Gonzalez / Behavioural Brain Research 222 (2011) 236245
DVR Associaon Areas
(Lateral/Ventral Pallium)
Hyperpallium
NCV PFC (NCL) NFL (Dorsal Pallium)
Entorhinal-like Areas
Piriform
Hippocampus
Cortex
Fig. 5. Limited connections between the avian hippocampus and association areas
in the dorsal ventricular ridge (DVR). The hippocampus receives visual input directly
from the hyperpallium and indirectly via proposed entorhinal-like areas; the dorso-
lateral portion of the hippocampal formation (DL), the parahippocampal area (APH),
and the dorsolateral corticoid area (CDL), or the entorhinal cortex, as dened by
Puelles et al. [120]. High-order visual input from the frontolateral nidopallium (NFL)
also reaches the hippocampus via the entorhinal-like areas. Other than the NFL, the
caudoventral nidopallium (NCV) is the only other area in the DVR providing input
to the hippocampus via the entorhinal-like areas. The caudolateral nidopallium
(NCL) the avian analogue of the mammalian prefrontal cortex (PFC) does not
project to the entorhinal-like areas or hippocampus, and does not receive pro-
jections from these structures. Other high-order association regions in the DVR
(nidopallium and mesopallium) are not connected to the entorhinal-like areas or
hippocampus. Olfactory input from the piriform cortex reaches the hippocampus
directly and indirectly via the entorhinal-like areas.
detected between the DVR and medial cortex (i.e., hippocampus)
in non-avian reptiles [34,130,176178]. Similar to birds, the medial
cortex only receives visual input from the dorsal cortex and olfac-
tory input from the lateral (piriform) cortex [130]. Consequently,
brain structures allocated to forming high-order associations in
mammals are intimately connected to the hippocampus, whereas
comparable association areas in the sauropsidian DVR are not. This
fundamental difference in brain organization undoubtedly inu-
ences how the avian brain processes information, including that
involved in episodic-like memory.
2.2.2. Neurophysiology
Consistent with the differences in brain organization observed
between mammals and birds, the neurophysiological properties of
the hippocampi also differ between these groups. Both modes of
hippocampal activity observed in mammals (i.e., theta and SWRs)
seem to be missing in birds during wakefulness and sleep (reviewed
in [25]), even though birds independently evolved sleep states in
most other respects similar to mammalian SWS and REM sleep
[25,179182]. Although less studied than the mammalian hip-
pocampus [15], most studies suggest that the avian hippocampus
does not generate a mammal-like theta rhythm during wakeful-
ness or REM sleep [25,183190]. A single study reported a slow
theta rhythm in awake pigeons (Columba livia), but unlike mam-
mals, this occurred during feeding and immobility, and not always
while walking [15,191]. Moreover, the authors did not report
whether it also occurred during REM sleep, as expected based
on mammals, and non-hippocampal sources for theta were not
ruled out ([25], see also [192]). Given these points and the absence
of reports of hippocampal theta in all other studies, including
those on pigeons, it remains unclear whether the reported theta
rhythm reects the same phenomenon as the mammalian hip-
pocampal theta rhythm. Moreover, neuroanatomical differences
between mammals and birds are also consistent with the absence
of a mammalian-like theta rhythm in birds. Projections from the
241
medial septum to the hippocampus, a pathway contributing to
the mammalian hippocampal theta rhythm (see Section 2.1.2),
are sparse or absent in birds, including pigeons [125,193195].
In addition to theta, SWRs have not been reported during any
Box 1
Why are bird brains organized differently from mammalian
brains?
Birds are a derived type of reptile. As such, the brain of early
birds probably resembled the general pattern exhibited by
extant non-avian reptiles; the dorsal cortex consisted of three
layers and the DVR was relatively small. Fossil endocasts
of the cranial cavity have been used to follow evolution-
ary changes in the gross volume of different brain areas in
both mammals and birds [18,19]. In terms of encephaliza-
tion and shape, fossilized endocasts of the cranial cavity from
dinosaurs suggest that expansion of the pallium occurred
after birds diverged from their dinosaur ancestors [18]. In liv-
ing birds, the hyperpallium and DVR ll two distinct areas
of the cranial cavity that expand dorsally along the mid-
line and laterally, respectively. Although the data is limited,
fossil endocasts suggest that the DVR enlarged well before
the hyperpallium. In Archaeopteryx lithographica, the earliest
known bird, expansion of the DVR, but not the hyperpallium,
is evident [199]. More recent birds from the Mesozoic show
further expansion of the DVR, but the hyperpallium does not
become evident in endocasts until the Cenozoic [19]. Thus, it
appears that birds progressively increased the size of the DVR
for an extended period of time before increasing the size of
the hyperpallium.
The proposed evolutionary sequence of events contributing
to encephalization of the avian brain may explain some of
the differences in pallial interactions with the hippocampus in
mammals and birds. Instead of expanding the dorsal pallium,
with its connections to the hippocampus, as did mammals,
birds initially elaborated on the DVR, a structure that may
have already been dedicated to forming some high-level asso-
ciations in their reptilian ancestors [138,200202]. As birds
elaborated further on the DVR, new associative processes
presumably became dependent on this structure, perhaps
including those related to PFC functions [25,202]. During this
time, as in modern non-avian reptiles and birds, the avian
hippocampus presumably continued to receive visual input
from the dorsal pallium, as well as olfactory input. The dor-
sal pallium expanded later to form the hyperpallium, perhaps
to enhance visual processing [203]. However, unlike the neo-
cortex, the role of the hyperpallium in forming multimodal
associations was limited, perhaps because such functions
were already performed by the DVR. Thus the early dedica-
tion of the sauropsidian DVR to performing most associational
processes may have shaped or constrained the ultimate orga-
nization of the avian brain.
But why did mammals elaborate on the dorsal pallium instead
of the DVR? Aboitiz et al. [175] suggest that this is attributable
to olfaction being a particularly important sense for early
nocturnal mammals. As a result, early mammals may have
elaborated on the olfactoryhippocampaldorsal cortex cir-
cuitry inherited from stem amniotes to process associational
information. As the importance of this associational circuitry
increased, it may have become benecial to recruit and
integrate other sensory modalities, especially vision when
mammals became diurnal. According to Aboitiz et al. [175],
this evolutionary sequence led to sensory information from
most modalities (lemnothalamic and collothalamic) reaching
the dorsal pallium (neocortex), wherein it is integrated to form
high-order multimodal associations before being conveyed to
the hippocampus to form episodic memories [175].
242 N.C. Rattenborg, D. Martinez-Gonzalez / Behavioural Brain Research 222 (2011) 236245
state using recording methods that readily detect them in mam-
mals [25,181,184,185,187,189191,196]. Of particular relevance
for this discussion of episodic-like memory, SWRs and theta were
not reported in hippocampal local eld potential recordings dur-
ing wakefulness, SWS, or REM sleep in black-billed magpies (P.
pica [189]), a food hoarding species which exhibits episodic-like
memory [5]. The apparent absence of neurophysiological rhythms
thought to mediate interactions between the hippocampus and
associative areas of the neocortex is consistent with the absence
of connections between the avian hippocampus and comparable
associative areas in the DVR.
3. Discussion
Collectively, the neuroanatomical and neurophysiological dif-
ferences between mammals and birds suggest that there may be a
fundamental difference between how episodic-like memories are
processed in each group. In contrast to the mammalian hippocam-
pus, the avian hippocampus does not seem to be privy to much
of the high-order multimodal associational information processed
in the DVR. Consequently, the visual and olfactory information
that reaches the avian hippocampus may be sufcient for what,
where, and when memory, at least in food hoarding birds, where this
has been established. However, components of daily experiences
processed in the DVR may not contribute to such episodic-like
memories. Although it is conceivable that information processed
in the DVR reaches the hippocampus via an unknown route, the
apparent anatomical differences are consistent with the absence
of neurophysiological rhythms implicated in coordinating the pro-
cessing of episodic memories between areas of the mammalian
brain. Specically, isolated from much of the DVR, including the
avian PFC, the avian hippocampus may not require the rhythms
used by the mammalian hippocampus to communicate with com-
parable structures in the neocortex.
The divergence in brain organization and activity exhibited
by mammals and birds raises several challenging questions. Does
information processed by the DVR contribute to episodic-like
memories? Is this information integrated during encoding and
retrieval with hippocampal information? Are episodic-like memo-
ries in birds less associative than those in mammals ([197], see also
[34,198])? Why did mammals and birds evolve such different brains
(Box 1)? Are there trade-offs associated with the different types of
brain organization? Are there differences in cognition attributable
to these differences in brain organization? Finally, despite the dif-
ferences between mammalian and avian brains, are there shared
traits that provide insight into fundamental processes contributing
to complex cognition? Attempts to answer these challenging ques-
tions may enhance our general understanding of how the brain
generates memories.
Acknowledgements
We thank John A. Lesku for valuable comments on an earlier
draft of the manuscript. This work was supported by the Max Planck
Society.
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