ARTICLE

Memoir of the Fukui Prefectural Dinosaur Museum 22: 1–12 (2023)© by the Fukui Prefectural Dinosaur Museum

ENDOCRANIAL ANATOMY OF THE CERATOPSIAN DINOSAUR
PSITTACOSAURUS LUJIATUNENSIS AND ITS BEARING ON SENSORY AND
LOCOMOTOR ABILITIESRina SAKAGAMI1, Soichiro KAWABE2,3, Soki HATTORI2,3, Wenjie ZHENG4 and Xingsheng JIN4
1

Department of Bioscience and Biotechnology, Fukui Prefectural University, 4-1-1 Matsuoka Kenjojima, Eiheiji,
Fukui 910-1195, Japan
2
Institute of Dinosaur Research, Fukui Prefectural University, 4-1-1 Matsuoka Kenjojima, Eiheiji, Fukui 910-1195, Japan
3
Fukui Prefectural Dinosaur Museum, 51-11 Terao, Muroko, Katsuyama, Fukui 911-8601, Japan
4
Zhejiang Museum of Natural History, Hangzhou, Zhejiang 310014, People's Republic of China
ABSTRACTPsittacosaurus is one of the dinosaurs with the highest number of skull morphologies analyzed. Psittacosaurus
lujiatunensis, in particular, is rich in morphological variation. Nevertheless, the intracranial neuroanatomy has not yet
been thoroughly analyzed. Hence, in order to understand the neuroanatomy of the ceratopsian P. lujiatunensis, twowell-preserved skulls of this species were analyzed using computed tomography (CT). Three-dimensional digital
endocasts of the cranial cavities and bony labyrinths were generated. They show that the cerebellar flocculi, which
had not previously been reported in P. lujiatunensis, is large for a ceratopsian. The enlarged cerebellar flocculi andwell-developed semicircular canals support the hypothesis that P. lujiatunensis had better gaze stability and balance
than other ceratopsians. The olfactory bulbs of P. lujiatunensis were relatively large compared to those of otherdinosaurs, suggesting that P. lujiatunensis possibly had a keen sense of smell. The cochlea was short compared tothat of the other dinosaurs, indicating that the P. lujiatunensis heard better at higher frequencies. This study provides
insights into the ecology and habits of P. lujiatunensis. The re-evaluation of the neuroanatomy of dinosaurs using
high-resolution CT analyses on well-preserved fossil specimens is crucial for a better understanding of their ecology.
Key words: digital endocast, endosseous labyrinth, Psittacosaurus lujiatunensis
坂上莉奈・河部壮一郎・服部創紀・鄭 文傑・金 幸生 (2023) 角竜類 Psittacosaurus lujiatunensis の脳・内耳形態と知覚・運動機能との関係．福井県立恐竜博物館紀要 22： 1‒12
Psittacosaurus は、最も多くの頭骨形態が解析されている恐竜の一つで，特に Psittacosaurus
Psittacosaurus lujiatunensis
lujiatunensis
は，形態的バリエーションが豊富である．一方で、その頭骨内部の神経解剖学解析はいまだ十分な精度で行われているとは言えない．そこで、2 個体の保存状態のよい P
P. lujiatunensis
lujiatunensis の頭骨を CT 撮影し、頭蓋腔及び骨迷路のデジタルエンドキャスト作成した．これらのエンドキャストの解析から，これまで角竜類
では報告されていなかった発達した小脳片葉が P
P. lujiatunensis
lujiatunensis に見られることが初めて確認された．小脳片葉の発達は視線の安定性に関係することから，PP. lujiatunensis
lujiatunensis は他の角竜類よりも視線の安定性や俊敏性に優れていた可能性がある．また，P.
lujiatunensis の嗅球は比較に用いた恐竜類の中では比較的大きく，鋭P lujiatunensis
い嗅覚を持っていたことが分かった．さらに，P.
lujiatunensis の蝸牛管は比較した恐竜類の中では短く，比P lujiatunensis
較的高い周波数を聞くことに適していたことが示された．このように，本研究は Psittacosaurus
Psittacosaurus の生態や習性に関する知見を改めて得るものとなり，保存状態の良い化石標本を用いた高解像度 CT 解析による恐竜の神経解剖学の再評価は，恐竜の詳細な生態を解明するためにも重要であることを示すものとなった．

INTRODUCTION

2007; Witmer and Ridgely, 2008). Among basal
non-neoceratopsian ceratopsians, Psittacosaurus has been thesubject of neuroanatomical works in which multiple digitalcranial endocasts were produced through computed
tomography (CT) analyses (Zhou et al., 2007; Bullar et al.,2019; Napoli et al., 2019). This is probably because thisspecies is one of the most abundant dinosaurs for which
cranial specimens can be found. Zhou et al. (2007) examined
three endocasts of Psittacosaurus lujiatunensis. They foundthat P. lujiatunensis had large olfactory bulbs and optic

Several previous studies have investigated theneurosensory function among ceratopsian dinosaurs (e.g.,
Brown, 1914; Hopson, 1979; Forster, 1996; Zhou et al.,Received September 22, 2022. Accepted May 26, 2023.
Corresponding author―Soichiro KAWABE
E-mail: kawabe_soichiro*yahoo.co.jp
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lobes. They also stated that the encephalization quotientswere higher than that of the theropod dinosaur
Tyrannosaurus. The results of Zhou et al. (2007) suggested
that Psittacosaurus likely exhibited complex behavior, had akeen sense of smell, and had acute vision. In addition, Zhou
et al. (2007) showed that Psittacosaurus possessed relatively
taller anterior semicircular canals than Protoceratops andmore derived ceratopsids, which suggests that this animal
could have been agile when trying to escape from predators.
Bullar et al. (2019) compared the inner ear morphology ofthree individuals of Psittacosaurus lujiatunensis at different
ontogenetic stages based on digital endocasts and discussedchanges in head postures through development. Napoli et al.
(2019) described the cranial endocast of Psittacosaurus
amitabha. They mentioned that a slightly ventrally-oriented
head posture was probable because the lateral semicircular
canal is slightly anterodorsally tilted.
Those studies provided valuable insights into theneuroanatomy of Psittacosaurus. However, the results of the
CT an a l y se s m a y h a v e b ee n imp a c te d b y th e s ta te ofpreservation of the specimens. In addition, with theenhancement of CT techniques and imaging, previously
overlooked anatomical features may now be detected. In thisstudy, we analyzed two well-preserved specimens of P.
lujiatunensis and conducted quantitative comparisons ofseveral endocranial anatomical features with other dinosaurs
to improve the understanding of the neuroanatomy andpaleoecology of P. lujiatunensis.
MATERIALS AND METHODSSpecimens and CT scanning
The specimens analyzed in this study include two skulls of
Psittacosaurus lujiatunensis (ZMNH M12414 and ZMNH
M12423) recovered from the Lower Cretaceous (Barremian)(Li et al., 2022) Lujiatun Beds of Yixian Formation in
Liaoning, China. They are housed in the Zhejiang Museum of
Natural History (ZMNH), Zhejiang, China. Threedimensional(3D) geometric morphometric analyses suggested that thethree psittacosaurid species from the Lujiatun Beds
(Hongshanosaurus houi, P. lujiatunensis, and Psittacosaurus
major) are actually taphomorphotypes of P. lujiatunensis(Hedrick and Dodson, 2013). We follow Hedrick and Dodson(2013) and assign the specimens to P. lujiatunensis. The
specimens were CT scanned with a micro-focus X-ray CT XT
H 320 (Nikon Solutions Co., Ltd.) at the College of Civil
Engineering and Architecture, Zhejiang University(Hangzhou, Zhejiang, China) (see Table 1 for scanparameters). We subsequently prepared the digital endocastsof the neurocranial cavities and bony labyrinths from theacquired CT images using the software Amira (v 2019.3,
Thermo Fisher Scientific; Waltham, MA, USA). Corfield etal. (2008) and Balanoff et al. (2016) provided detailed
methods to prepare and examine the endocast models.

TABLE 1. Specimens used for this study and the relevant scanparameters.

Generally, reptile brains – including presumably those of
non-theropod dinosaurs – do not fill the endocranial cavity(Hopson, 1979). Furthermore, it is known that the distance
between the brain and the cranial bones forming the cranial
cavity, i.e., the shape difference between the cranial endocast
and the actual brain, increases with development among
nonavian archosaurs (Jirak and Janacek, 2017). Therefore,
the endocasts do not provide an accurate picture of the brain
morphology in these animals. Particularly, the posterior partof an endocast tends to appear larger than that of the actual
brain in reptiles (Hopson, 1979; Watanabe et al., 2019).
Despite these limitations, endocasts still provide a premiersource of information on brain morphology in extinct species.
Measurements
To assess the olfactory bulb size of P. lujiatunensis, theratio of the greatest diameter of the olfactory bulb to thegreatest diameter of the cerebral hemispheres (i.e., olfactoryratio) was measured in the digital brain endocast of ZMNH
M12414. Then, the common logarithm of the ratio was taken
following Zelenitsky et al. (2009). Next, the ratio must be
standardized to the log10 body mass to compare the log10
olfactory ratio with those in other dinosaurs.
The ontogenetic stage for each specimen was estimated byusing the following regression equation established by Zhao
et al. (2014), where X is the age in years, and Y is the skull
length (from the posterior end of the occipital condyle to theanterior end of the rostrum) in mm:
Y = 15.8 X + 32.2
Subsequently, the body mass was calculated following
Erickson et al. (2009), where the body mass is in kg and theage in years:
body mass = 37.38 × exp (0.55 × age) / (37.38 + (exp(0.55 ×age) – 1))
To assess the degree of development of the semicircular
canals of P. lujiatunensis, the ratio of the height of theanterior semicircular canal (ASC) to its external diameter andthe ratio of the total height of the posterior semicircular canal(PSC) to the height of the PSC below the plane of the lateralsemicircular canal were calculated for ZMNH M12414 andM12423, following Domínguez Alonso et al. (2004) (Fig. 1;
Table 2). Then, both ratios were compared with the results of
Sakagami and Kawabe (2020) (Table 3).
The endosseous cochlear duct length (CL) for P.
lujiatunensis was measured to estimate the best frequency ofhearing and the hearing limit. The best frequency of hearing

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TABLE 2. Measurements and calculated values used in this study.

Relative ASC height, height of the anterior semicircular canal/external diameter of anterior semicircular canal; Relative PSC height, height from the baseof the posterior semicircular canal to the plane of the lateral semicircular canal/height of the posterior semicircular canal.

lujiatunensis were compared with those in the other taxa
treated by Sakagami and Kawabe (2020) and Knoll et al.
(2021) (Table 3).
RESULTS

FIGURE 1. Measurement points for the endosseous labyrinth.

was calculated by the following regression equation proposed
by Gleich et al. (2005), where X is the basilar papilla length,
and Y is the best frequency of hearing:Y = 5.7705 e-0.25X
The basilar papilla lengths were calculated from the CL,
based on the estimation of Gleich et al. (2005) that the basilar
papilla length corresponds to two-thirds of the CL. The
hearing limit was then determined following the regression
equation by Gleich et al. (2005), in which X is the best
frequency of hearing and Y is the highest frequency ofhearing:
Y = 1.8436 X + 1.0426
Finally, the best and highest frequencies of hearing for P.

ZMNH M12414 (Fig. 2) is well-preserved. In contrast,
ZMNH M12423 (Fig. 3) appears to have sufferedcompressive deformation from dorsoventral forces
approximately in the middle of the skull. A large
dorsoventral crack extends through the anterior end of theleft orbit and the right lateral end of the occiput. However,these deformation and crack do not significantly affect thearea around the braincase. Based on the skull length of 134.6
mm, the ontogenetic stage and body mass of ZMNH M12414
were estimated to be six years and 18.4 kg. The skull lengthof ZMNH M12423 is 102.7 mm, from which the age andbody mass were estimated as four years and 9.1 kg. The
olfactory bulb of ZMNH M12423 could not be reconstructed
due to the crack (Fig. 3), whereas that of ZMNH M12414
was reconstructed successfully (Fig. 2). In dorsal view, theolfactory bulb of ZMNH M12414 bifurcates to form an angleof approximately 17 ° with the midline anterior to the olfactory
tract. The olfactory tract extends along the ventral surface ofthe frontals and gradually transitions to the cerebrum
posteriorly (Fig. 2). The olfactory ratio was 0.57 (Table 2).
The cerebral shapes in ZMNH M12414 and M12423
resemble those of Psittacosaurus lujiatunensis (Zhou et al.,2007) and Psittacosaurus amitabha (Napoli et al., 2019).
Their relative sizes are smaller than those of coelurosaurian
theropods and hadrosaurid ornithopods (Evans et al., 2009;
Witmer and Ridgely, 2009; Balanoff et al., 2018). Posterior
to the cerebrum, the dorsal part of the hindbrain expands
posterodorsally in each specimen (Figs. 2 and 3), supposedly
due to dural sinus, as seen in P. lujiatunensis and P.
amitabha (Zhou et al., 2007; Napoli et al., 2019). The optic
lobe is expanded laterally in ZMNH M12414 (Fig. 4), while
it is unobservable in ZMNH M12423, probably due to thetaphonomic dorsoventral compression. The lateral expansionof the optic lobe is also recognized as a bulbous protrusion

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TABLE 3. Proportions of the endosseous labyrinth and estimated hearing frequencies of selected dinosaurs.

Relative ASC height, height of the anterior semicircular canal/external diameter of anterior semicircular canal; Relative PSC height, height from the baseof the posterior semicircular canal to the plane of the lateral semicircular canal/height of the posterior semicircular canal. “Best frequency of hearing” and“High frequency hearing limit” were calculated following the method of Gleich et al. (2005).

on the endocast in P. lujiatunensis (Zhou et al., 2007), in
contrast to the situation in P. amitabha (Napoli et al., 2019).
The cerebellar flocculus (floccular lobe) extends laterally to
cross the plane defined by the ASC in both specimens. It is
not visible on the endocast of neoceratopsians such as

Protoceratops, Pachyrhinosaurus, Anchiceratops, andTriceratops (Brown, 1914; Hopson, 1979; Forster, 1996;
Witmer et al., 2008). Its presence on the endocast of
Psittacosaurus has not been recognized in earlier studies(Zhou et al., 2007; Napoli et al., 2019), but differences

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Figure 2. Cranial endocast (A–C) and skull (D–F) of ZMNH M12414 in left lateral (A, D), ventral (B, E), and dorsal (C, F) views. Cranial endocast,cranial nerves, carotid artery, and endosseous labyrinths are represented by pink, yellow, red, and purple colorings, respectively. Abbreviations: car,carotid artery; cer, cerebral hemisphere; flo, cerebellar flocculus; lab, labyrinth; ob, olfactory bulb; V, trigeminal nerve; VII, facial nerve; VII,
vestibulocochlear nerve; IX-XI, shared canal for glossopharyngeal, vagus, and accessory nerves; XII1-2, first and second branches of hypoglossal nerve;
XII, hypoglossal nerve.

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RINA SAKAGAMI, SOICHIRO KAWABE, SOKI HATTORI, WENJIE ZHENG AND XINGSHENG JIN

FIGURE 3. Cranial endocast (A–C) and braincase (D–F) of ZMNH M12423 in left lateral (A, D), ventral (B, E), and dorsal (C, F) views. Color scheme
and abbreviations as in Fig. 2.

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Endosseous labyrinth

FIGURE 4. Optic lobe and cerebellar flocculus of ZMNH M12414 inright lateral view. Only the cranial endocast is shown for clarity.

regarding the preservation of the specimens or the CT image
resolution may have allowed the identification of optic lobes
in this study.
Only the internal carotid arteries could be reconstructedfrom the vascular system in both specimens. The internal
carotid arteries extend lateroventrally from the ventral end of
the pituitary (Figs. 2 and 3).
Cranial nerves
The cranial endocast includes the roots of some cranial
nerves (CNs) and the accompanying assemblage of soft
tissues, such as blood vessels. However, because the latter isdifficult to discern independently in endocasts, we will focus
on the morphology of the cranial nerves here.
The canals for the optic, oculomotor, trochlear, andabducens nerves (CNs II–IV, VI) are not visible in thespecimens due to preservation. In lateral view, the canal forthe trigeminal nerve (CN V) projects anterolaterally from thearea posteroventral to the cerebrum at the level of the LSC of
the inner ear. This nerve exits through one opening on thelaterosphenoid-prootic suture. In ZMNH M12423, the canalfor the facial nerve (CN VII) that extends anterolaterally toexit through the prootic is preserved. The canal for thevestibulocochlear nerve (CN VIII) extends from justposterior to the facial nerve canal laterally to connect withthe vestibule of the inner ear. The canal for theglossopharyngeal vagus, and accessory nerves (CNs IX–XI)
is also observed as a single trunk. This structure is known inmany amniotes and is typically called the vagal canal(Sampson and Witmer 2007; Witmer et al. 2008). The vagal
canal extends posteroventrally to open in the otoccipital in
ZMNH M12423. The two canals for the hypoglossal nerves(CN XII) are positioned posterior to the vagal canal andextend posterolaterally.

The labyrinths of the inner ear are preserved on both sides
of ZMNH M12414 (Figs. 2, 5) and ZMNH M12423 (Figs. 3,6) but cannot be fully reconstructed in ZMNH M12423 inwhich the ASC is only partially discernible in the CT images,
possibly due to poor preservation. The inner ear is locatedposterolateral to the cerebellum. The ASC is dorsoventrally
taller than the PSC, contrary to the conditions in
Anchiceratops, Pachyrhinosaurus lakustai,
Pachyrhinosaurus perotorum, and Triceratops sp. (Brown
1914; Witmer and Ridgely 2008; Tykoski and Fiorillo 2013;
Sakagami and Kawabe 2020) in which they have roughly thesame height. In this regard, the ASC of P. lujiatunensis is
more reminiscent of the situation in theropods such as
Tyrannosaurus (Witmer and Ridgely 2009). In lateral view,
when the LSC is oriented horizontally, the ASC curves
unevenly from its dorsal extremity to the anterior tip of theLSC, and the PSC extends ventrally slightly beyond the levelof the LSC. The cochlear duct is 5.07 mm tall dorsoventrally
on the left side of ZMNH M12414 and 4.33 mm on the left
side of ZMNH M12423. Based on these lengths, the best
frequency of hearing is estimated to be 2479 Hz for ZMNH
M12414 and 2804 Hz for ZMNH M12423 (Table 2). The
quotient of dividing the height by the external diameter of the
ASC is 1.353 in ZMNH M12414 and 1.381 in ZMNH
M12423 (Table 2). The quotient of dividing the total heightof the PSC by the portion of it that extends ventrally beyond
the LSC plane is 0.416 in ZMNH M12414 and 0.428 in
ZMNH M12423 (Table 2). In lateral view, the angle between
the palatal plane and the LSC plane is about 15º and 5º in
ZMNH M12414 and M12423, respectively.
DISCUSSION
Head posture
The LSC provides valuable information for estimating thehead posture of extinct animals since the alert head posturesof extinct animals can be somewhat deducted frompositioning the LSC horizontally (Duijm 1951). In this study,
the angles between the plane of the LSC and the palatal plane
were measured and considered as the head posture. The
results showed that ZMNH M 12414 had a palatal plane tilted
15º ventrally from the horizontal plane (Fig. 7). Bullar et al.
(2019) estimated the head posture of three Psittacosaurus
lujiatunensis at different developmental stages. They foundthat a hatchling individual (IVPP V15451), estimated to beless than one year old, had a 38º head posture, a juvenile
individual (IVPP V22647), estimated to be approximately
two years old, had a 25º posture, and a 10-year-old adult(IVPP V12617) was tilted 15º. The head posture of ZMNH
M12414, which is estimated to be roughly adult at six yearsof age, at 15º, is consistent with the results shown by Bullar
et al. (2019) for IVPP V12617.

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FIGURE 5. Left endosseous labyrinth of ZMNH M12414 in lateral (A), posterior (B), and dorsal (C) views. Abbreviations: ASC, anterior semicircular
canal; CC, cochlea; CRC, crus commune; LSC, lateral semicircular canal; PSC, posterior semicircular canal; VE, vestibule of inner ear.

FIGURE 6. Left endosseous labyrinth of ZMNH M12423 in lateral (A), posterior (B), and dorsal (C) views. Abbreviations as in Fig. 5.

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FIGURE 7. The possible head posture of Psittacosaurus (ZMNH
M12414) when the lateral semicircular canal is Earth horizontal. The
solid and broken lines indicate the palatal plane and the plane of thelateral semicircular canal, respectively.

On the other hand, the head posture of ZMNH M12423,
estimated to be roughly adult at four years of age, issuggested as only 5º below the horizontal plane. Considering
the results of Bullar et al. (2019), the head posture of ZMNH
M12423 would be expected to be between 15º and 25º, but
the values obtained in this study deviate significantly fromthis range. This may be due to the deformation of therostrum, which is bent dorsally to the neurocranium.
However, the degree of deformation of ZMNH M12423 is
not extreme, and even in the absence of deformation, thehead posture would not appear to be as angled as describedby Bullar et al. (2019). Change in head posture during thedevelopment of P. lujiatunensis would become clearer withthe study of well-preserved specimens.
It should be noted that a certain degree of error in the
LSC-based head posture reconstruction has been reported
successively in recent years (Marugán-Lobón et al. 2013;
Berlin et al. 2013; Coutier et al. 2017). Although moredetailed discussion is needed to determine whether this angle
accurately reflects the posture of P. lujiatunensis in its
natural habitat, it is still meaningful to use the LSC as astandard for intraspecific comparison of head postures, and it
is valuable for understanding how the head posture of P.
lujiatunensis changed during development.
Stabilization of gaze and posture
The enlarged cerebellar flocculi observed in this study area unique feature found only in P. lujiatunensis and not in any
other ceratopsians (Brown 1914; Hopson 1979; Zhou et al.
2007; Witmer and Ridgely 2008; Tykoski and Fiorillo 2013).
Such enlarged cerebellar flocculi are also known in extant

FIGURE 8. Comparative proportions of ASC and PSC. Scatterplots ofthe percentage of the PSC situated inferiorly to the plane of the LSC
versus ratio height/width of the ASC in ceratopsians.

birds, non-avian theropods, and pterosaurs (Witmer et al.
2003; Witmer and Ridgely 2009; Walsh et al. 2013; Ballell et
al. 2021). Witmer et al. (2003) argued that the size of thecerebellar flocculus (relative to total brain mass) is linked tothe ability to stabilize gaze. Hence, Witmer et al. (2003)
assumed that pterosaurs possibly had better gaze stabilization
due to their enlarged cerebellar flocculi. On the other hand,
Walsh et al. (2013) found no significant relationship between
the relative size of the flocculus (floccular fossa volume
relative to endocranial volume) and flight mode classificationin extant birds and concluded that the floccular fossa size is
not a proxy for flying control. Walsh et al. (2013) also foundthat obligate terrestrial birds such as emus had slightly larger
flocculi than flying birds – possibly due to the unstable
nature of bipedal locomotion. Walsh et al. (2013) alsosuggest that the enlarged flocculi observed in non-avian
dinosaurs and pterosaurs are possibly related to the evolutionof bipedal terrestrial locomotion because it requires bettergaze stability than quadrupedal locomotion. In the case of P.
lujiatunensis, the enlargement of the cerebellar flocculi, in
combination with the well-developed semicircular canals(discussed below), may suggest that psittacosaurs possessed abetter sense of gaze stabilization than other ceratopsians.

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FIGURE 9. Best frequency of hearing for selected dinosaurs.

The relationships between the morphology of thesemicircular canals and the sense of balance, the agility oflocomotion, and the stabilization of gaze have been discussed(e.g., Spoor et al. 2007). In order to assess the degree ofsemicircular-canal development of an avialan theropod,
Archaeopteryx, Domínguez Alonso et al. (2004) investigated
the ratios between the height and external diameter of the
ASC and the percentage of the height of the PSC that extends
below the plane of the LSC. The present study comparedthese ratios with those of ceratopsians (Table 3). These ratios
for ZMNH M12414 and M12423 were added to the dataset of
Sakagami and Kawabe (2020) (Fig. 8). ZMNH M12414 andM12423 plot in the region showing a relatively tall ASC anda ventrally projecting PSC. This is consistent with Sakagami
and Kawabe’s (2020) results, in which basal ceratopsians,
including P. lujiatunensis, had well-developed ASC andgreater gaze stability than derived ones.
Hearing ability
In extant animals – including mammals, birds, and reptiles– the CL has been used as an indicator of hearing ability
because the length of the basilar papilla within the cochlear
duct is correlated with hearing frequency (see Walsh et al.
2009). Similarly, the CL has been used to estimate thehearing ability of extinct animals including dinosaurs (Evanset al. 2009). In this study, we added the data of two
specimens of P. lujiatunensis into Sakagami and Kawabe’s(2020) dataset and compared them with the hearing
frequency of a sample of dinosaurs (Fig. 9). When comparedwith other non-avian dinosaurs, the best frequency of hearing
for P. lujiatunensis is relatively high. However, it must be
noted that CL values for ZMNH M12414 and M12423 were
well outside the ranges of those employed to empiricallyderive the regression equation in Gleich et al. (2005), which
may lead to erroneous estimation of the best frequency ofhearing.

FIGURE 10. Scatterplot of olfactory ratio versus body mass foralligators, ceratopsids, a pachycephalosaurid, ornithopods, andtheropods. The line is the least-squares linear regression line (y =0.1237x+1.316) for theropods as calculated by Zelenitsky et al. (2009).

Olfactory bulbs and sense of smell
The relative degree of development of the olfactory bulb is
supposed to indicate the acuity of the sense of smell in extant
mammals and archosaurs based on a positive correlation
between the olfactory bulb size and olfactory acuity (Cobb
1960; Zelenitsky et al. 2009). The olfactory ratio of ZMNH
M12414 is compared with those of theropods, otherdinosaurs, and alligators in a scatter plot of log10 olfactoryratio against log10 body mass provided by Zelenitsky et al.
(2009) and Sakagami and Kawabe (2020). ZMNH M12414
plots considerably above the regression line (Fig. 10),indic a ting tha t the a c uity of the s e ns e of s me ll of P .
lujiatunensis was higher than the average of the taxa
considered in the analysis. Our results are consistent with theobservations by Zhou et al. (2007), according to which P.
lujiatunensis has an enlarged olfactory bulb. In contrast to P.
lujiatunensis, late-diverging ceratopsians (Pachyrhinosaurus
and Triceratops) are regarded as exhibiting relatively small
olfactory bulbs (Witmer and Ridgely 2008; Sakagami and
Kawabe 2020). The present study quantitatively demonstrates
that P. lujiatunensis has a relatively large olfactory bulb,
which supports a more acute sense of smell than in derived
ceratopsians.
CONCLUSIONSIn this study, cranial endocasts of Psittacosaurus

ENDOCRANIAL ANATOMY OF PSITTACOSAURUS

lujiatunensis were reconstructed by CT analyses of two new
specimens. Our examination revealed enlarged cerebellar
flocculi, which have not been reported in any otherceratopsian. The enlarged cerebellar flocculi imply bettergaze stability. This observation is consistent with themorphometry of the semicircular canals, in which the ASC isrelatively tall and the PSC projects more ventrally.
Furthermore, the orientation of the LSC and the relatively
large olfactory bulb indicate a slightly downward headposture and a relatively acute sense of smell, respectively. In
addition, the best frequency of hearing of two specimens of
P. lujiatunensis based on the cochlear length were 2479 and
2 8 0 4 Hz , wh i c h ma y h av e b e e n re la tiv ely high w he ncompared to other dinosaurs.
Thanks to high-resolution CT analyses, this study
substantially informs the study of the ecology and habits of
P. lujiatunensis. Furthermore, it demonstrates that thedevelopment of CT techniques enables re-assessment of theneuroanatomy in fossil taxa and helps collect more data inquality and quantity, leading to a better understanding of thebiology of said taxa.
ACKNOWLEDGEMENTS
We thank the College of Civil Engineering andArchitecture, Zhejiang University staff for assisting in
conducting CT analyses and the researchers and staff of theZhejiang Museum of Natural History and Fukui Prefectural
Dinosaur Museum for providing information about the
specimens. The Institute of Dinosaur Research, Fukui
Prefectural University members provided helpful comments
and suggestions for this study. Dr. Fabien Knoll(ARAIDFundación Conjunto Paleontológico deTeruel-Dinópolis) and Dr. Qi Zhao (Key Laboratory of
Vertebrate Evolution and Human Origins, Institute of
Vertebrate Paleontology and Paleoanthropology, Chinese
Academy of Sciences) provided helpful reviews. The authors
also thank Takuya Imai (Institute of Dinosaur Research of
Fukui Prefectural University) for the English language
review. This work was supported by JSPS KAKENHI Grant
Number 21K03737.
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