SJÄLVSTÄNDIGT ARBETE I BIOLOGI

15hp, VT2014

Evolution and function of the vertebrate cerebellum: a review of existing literature

across different organisms.

Author: Annika JohanssonSupervisor: Niclas Kolm, Department of Zoology/Ethology

Ethology 2

Sammanfattning

Evolution och funktion av cerebellum hos vertebrater: en sammanställning av befintlig

litteratur över olika organismer.

Länken mellan fysiologi och adaptivt beteende är idag ett högaktuellt område inom etologi och evolutionsbiologi.

Särskilt centrala nervsystemets roll är intressant för att förstå vilka mekanismer som ligger bakom djurs beteende

och hur de anpassats under evolutionär tid. En intressant men understuderad struktur i vertebrathjärnan är

cerebellum. Cerebellum är den morfologiskt mest varierande strukturen i hjärnan. Hittills finns ingen

litteratursammanställning över om variationen i cerebellums morfologi påverkar komplexa beteenden och vilka

evolutionärekologiska faktorer som är associerade till den befintliga morfologiska variationen. Syftet med studien är

att sammanställa existerande litteratur om cerebellums funktion, ekologi och evolution. Resultaten tyder på att en

komplex cerebellum är kopplad till evolutionärt yngre arter, som lever i en omväxlande, ofta 3-dimensionell miljö,

vilket kräver avancerade beteendemönster och ökade kognitiva förmågor. Även inlärning och sociala interaktioner är

kopplade till en ökad komplexitet av cerebellum. Sambandet ser liknande ut över olika taxa. För en mer heltäckande

bild av cerebellums funktion krävs främst beteendestudier. Särskilt kunskap om cerebellums betydelse för sociala

beteenden och kognition saknas i stort i fältet. Artificiella selektionsförsök saknas hos alla taxa.

IntroductionThe link between vertebrate neuroanatomy and adaptive behavior is of continuously

growing interest in ethology and evolutionary biology. Advanced and complex behaviors are

strongly associated with the constitution of the central nervous system (Striedter, 2005;

Boogert et al. 2011; Oliveira, 2013; Bshary, 2014). The relative size of the whole brain or

particular areas in the brain is crucial for the complexity of behavior and reflects the

importance of behavior sequences (Jerison, 1973; Bernard, 2003; Striedter, 2005;

Shettlewoth, 2010; Bshary, 2014). For instance, brain size increases in group living primates

since social intelligence is required to live in groups (Dunbar & Schultz, 2007). Therefore, the

link between adaptive behavior and neurodensity, brain size and structure is an important

discipline in biological research of the link between neuroanatomy and behavior. Till now,

especially comparative analyses, across species, of the central nervous system have been of

particular interest to determine what aspects of the central nervous system that are conserved

and what aspects are highly diverse in relation to animal behavior. This knowledge is of great

importance to understand how behavior can evolve and adapt in relation to their physical and

social environment (Shettleworth, 2010).

2014

Ethology 3

The cerebellum, commonly known as “the little

brain”, is a sub-structure in the vertebrate brain and

was previously thought to only control balance,

motor skills and coordination of movements

(Striedter, 2005; Thach et al. 1992, 1996), but has

recently been implemented also in cognition (Healy

et al. 2010; Thach, 1996).

The cerebellum exists in all vertebrate, with one exception, the hagfishes (Striedter, 2005;

Butler & Hodos, 2005). All other species from every vertebrate class, from lampreys to

mammals has a cerebellum (Striedter, 2005; Butler & Hodos, 2005). The hagfishes and

lampreys were diverged almost 550 Mya (Hickman et al. 2012). In 500 Mya of vertebrate

evolution, the cerebellum has developed into an enormous variation of sizes, shapes and sub-

structures across the vertebrates. In fact, no other brain structure exhibits such diversity in

morphology, even though other structures, e.g. the telencephalon, are evolutionarily older

than the cerebellum (Butler & Hodos, 2005). Cerebellum is a structure that is distinguishable

from the other parts of the brain with its large-scale taxonomic variation in complexity among

all vertebrates (Butler & Hodos, 2005). However, the cerebellum has been given surprisingly

little attention from an evolutionary perspective in modern scientific work, with respect to its

unique morphological variance and diverse functional roles in animal behavior.

Among the enormous variation in the morphology of cerebellum, especially two

morphological characters are of interest, cerebellum size and cerebellum foliation. These

morphologies are particularly variable in a way that could co-vary with adaptive changes.

At the large scale taxonomic level there is a tendency that lower vertebrates, lampreys

and amphibians, have a less complex cerebellum than higher vertebrates, like birds and

mammals (Butler & Hodos, 2005; Meek, 1992). Lampreys, cartilaginous and bony fishes,

amphibians and reptiles tend to have a relatively smaller cerebellum in proportion to whole

brain size, with a smooth unfolded surface, while birds and mammals have a relatively large

and highly foliated cerebellum (Butler &Hodos, 2005; Meek, 1992). More recently evolved

species within the groups of ancestral vertebrates often have a more complex cerebellum in

similarity with higher vertebrates (Butler & Hodos, 2005; Meek, 1992). The variation in

cerebellum morphology does not only correlate with phylogenetic relationships, but often

2014

Ethology 4

with lifestyle (Yopak et al. 2007; Lisney et al. 2008; Bennett & Harvey, 1985; Pollen et al.

2007). The most ancestral mammals, the monotremes echidna and the duckbilled platypus,

have a larger and more foliated cerebellum, than some more recently evolved primates. This

has been suggested to be due to their advanced detection of prey (Stridter, 2005; Rose, 2004).

In a specific group of teleosts, the mormyrid electric fishes, the relatively largest cerebellum

among all vertebrates are found. This enlarged so called “gigantocerebellum” (Meek et al.

2008) occupy over 50 % of the total brain mass (Striedter, 2005; Butler & Hodos, 2005; Rose,

2004; Meek et al. 2008), and the weight is nearly 80 % of the total brain weight (Butler &

Hodos, 2005). In contrast, the human cerebellum is relatively small and only occupies 10 %

of the total brain mass (Kandel et al. 2013).

Besides the enormous variation in cerebellum gross morphology, there are two

characteristics of the cerebellum that all vertebrates have in common. First, the neurons of the

cerebellum are the most densely packed cells in the whole vertebrate brain. The cerebellum

holds more than half of the total number of neurons (Kandel et al. 2013; Barton, 2012), and

the smaller the animal the more densely they are packed. In mammals, whales and elephants

have 800- 1,100 cells per cubic µm in the granule cell layer, and small rodents have 2,500-

3,200 cells per cubic µm. This pattern, with increasing neuron density in the cerebellum of

smaller species, has also been observed in birds (Butler & Hodos, 2005). As mentioned

previously, the human cerebellum is relatively small, but it holds more than half of the total

number of neurons in the human brain (Kandel et al. 2013), and up to four times as many than

in the neocortex in other mammals (Barton, 2012). This suggests that a specific number of

neurons are required to control and regulate the functions of cerebellum, and to pack the

neurons more densely could be one strategy when increasing the overall volume of the

structure (or the whole brain), is not an evolutionary possibility. Second, the cerebellum has a

very conservative neuroanatomical pattern, and exists of relatively few sub-structures which

are shared in all vertebrates (I will not treat these sub-structures in detail in this report but

more information can be found in Butler & Hodos, 2005).

The relative importance of a specific behavior or a behavior pattern can be linked to the

relative size of the brain structure controlling it (Barnard, 2003). As mentioned previously, the

role of the cerebellum seems to be of great importance among vertebrates, since when there is

not room enough to enlarge its size, it becomes more foliated or its neuron density increases

(Kandel et al. 2013; Iwaniuk et al. 2006). There is a pattern in support of a trade off in

2014

Ethology 5

relative brain structure size and foliation among all vertebrates (Striedter, 2005; Yopak et al.

2007), and therefore a large cerebellum does not always mean a high degree of foliation or

vice versa (Iwanuk et al. 2009). The foliation of the cerebellum has also increased with

evolutionary time in certain lineages (Yopak et al. 2007; Lisney et al. 2008; Butler & Hodos,

2005; Iwaniuk et al. 2006), which strengthens the theory of cerebellum as a structure of great

importance.

In vertebrates, behaviors are controlled by the central nervous system. The complexity of

a behavioral pattern is a reflection of the complexity of the organization controlling it

(Barnard, 2003). This is true both for the whole brain and for the specific structures (Striedter,

2005). Interestingly, despite the simplicity in neural circuits, a number of studies have

included the cerebellum as an important structure also for various types of complex behavior.

However, there exists no real consensus regarding the causes and consequences of the

enormous variation in cerebellum morphology that exists among vertebrates even though at

least some of the morphological variations in the cerebellum appear to be matched by

variation in behavior (Butler & Hodos, 2005; Iwaniuk et al. 2009; Yopak et al. 2007).

The link between the morphology, function and evolution of a given brain structure is

usually studied using comparative analyses (Yopak et al. 2007; Gonzales-Voyer et al. 2009),

lesion studies (Thach et al. 1992) or trough artificial selection experiments (Falconer &

Mackay, 1996; Kotrschal et al. 2013). To fully understand and get a complete picture of the

link between physiology, adaptive behavior, phylogenetic relationships and the evolution of

the whole brain, or a specific structure, results from varies kind of studies must been taken

into account for a correct and proper conclusion.

So far no summary of the number of potential functions controlled by the cerebellum

exists, particularly in light of how different taxa may differ in cerebellum function and how

different methods (i.e. comparative analyses, lesion analyses and artificial selection

experiments), might reveal different patterns. My aim with this study is to provide an

overview of the functions that the cerebellum has been shown to be involved in, across

different taxa. Which functions are associated with a larger, more complex cerebellum? What

aspects of behavior are associated with cerebellum size and complexity? Which evolutionary

ecological factors is cerebellum variation linked to? Are the patterns similar across taxa?

2014

Ethology 6

I will summarize existing and available literature on cerebellar function, evolution and

ecological variables that are associated with variation in cerebellum morphology. My

literature study will contribute to the identification of how future research project can be

designed to widen our knowledge of the link between brain morphology and behavior at all

taxonomical levels.

MethodsIn order to summarize what we know today about cerebellums function, ecology and

evolution I sampled existing research on cerebellum function, ecology and evolution in all

vertebrates besides hagfishes. I only used peer reviewed research articles published in

established journals in the field of ethology, biology, zoology, neuroscience, behavioral

science, psychology, fisheries, evolutionary biology and ecology. To find these I searched for

relevant articles on Web of science and Google scholar. I wanted to know which different

functions cerebellum is involved in, and which ecological factors that could play a role to the

existing variation in cerebellum morphology and function. For this, I did a basic search for

topics such as: cerebellum ecology, cerebellum function, or cerebellum behavior. I also

refined the results by adding the specific taxa of animals, lampreys, chondrichthyans,

osteichthyes, amphibians, reptiles, birds and mammals. When I needed to be even more

specific I searched for a specific behavior in each taxa, i.e. tool use, or learning. In my search

for lesion studies, I searched for i.e. lesion and cerebellum and behavior, both generally and

for each specific taxa. I have searched both Web of science and Google scholar with exactly

the same keywords and topics. I excluded all studies that were not linked to ecology,

locomotion, behavior or function.

In table 1 I present all the studies I found that investigated some aspect of cerebellum

function. In the table I list following information: class, number of species together with

group of animals and families included in each study. I also present which type of data on

cerebellum morphology that was used in each study (relative size as a proportion to the whole

brain, foliation degree, size of folia, neural circuits, neural activity, chemical manipulation,

lesion or flocculus size). The cerebellar flocculus is a specific part of the cerebellum situated

at the dorsal side, and this part was for instance thought to be the origin of the flying ability in

Pterosaurs and early birds (Walsh et al. 2013). I also present the factor that the cerebellum

data of each study was linked to. Here I list also the direction of the association between the

2014

Ethology 7

factor and the cerebellum data (i.e. positive (+) or negative (-) association between the

cerebellum data and the factor). To get a good overview of the number of different areas, the

characteristic of the factor (ecology, behavior, function or locomotion), is also presented.

I consider a more complex cerebellum to be of relatively large size or of a high degree of

foliation, or a combination of both variables, while a less complex cerebellum is of relatively

small size and/or with a smooth unfolded surface (Striedter, 2005; Butler & Hodos, 2005).

For included papers on the association between habitat dimensionality variation and

cerebellum, I consider a 3-dimensional habitat to be more complex than 2-dimensional

habitats in line with Yopak et al. (2007) and Bennett & Harvey (1985). In aquatic

environments, I consider bentopelagic and pelagic zones, referred to as coral reefs,

coastal/pelagic or oceanic environments as 3-dimensional habitats, and to be more complex

than benthic and benthopelagic zones which consist of demersal areas near the sea floor or the

bathyal zone, in line with Yopak et al. (2007). In the terrestrial environment, I consider

arboreal and aerial habitats and habitats associated with aquatic environments (e.g. swamps

where an animal spends time both on water and on land), to be more complex than 2-

dimensional environments near the ground, in line with Bennett & Harvey (1985).

Results

My literature searches resulted in a total number of 57 comparative- and lesion analyses

and no artificial selection experiments (Table 1). The relevant literature found was very

unevenly distributed across the taxa. For instance, I found only one study on cerebellum in

lampreys and the results from the search within amphibians and reptiles were also very few in

numbers. I only found three reports on the function of cerebellum in these two groups, one

lesion study in reptiles and in amphibians I found one comparative analyses and one study on

neural circuits. Among the chondrichtyans, the cartilaginous fishes, I found four comparative

analyses, two lesion studies, and one study on neural circuits. Among the osteichtyes, the

bony fishes, I found eight comparative analyses and three lesion studies and two studies on

neural circuits within this group. In the class aves I found nine comparative analyses and two

lesion studies. In the class mammalia I found four comparative studies, 14 lesion studies and

twelve studies on neural circuits. All the mammalian research in cerebellar function was

2014

Ethology 8

mostly done in rodents or humans with cerebellar damages. Only a few results on the link

between behavior and cerebellum complexity was found.

In the cartilaginuos fishes, both in holocephalans and elasmobranchii, all studies detected

a positive association between complexity in cerebellum and complexity in habitat, range of

migration, swimming speed, and overall activity, depth of habitat, hunting mode and social

behavior (Table 1). In holocephalans the patterns was reversed in respect to one factor. Here,

there was a negative association between a complex cerebellum and habitat depth. One

species among the elasmobranchi differed from the others as regards ecological factors and

locomotion, since it was a slow moving filter feeder with a relatively large and highly foliated

cerebellum. Whereas it does wide ranging movements and is known for its ability to vertical

migration up to one mile deep, which are traits that co-vary with a more complex cerebellum.

In bony fishes, as in cartilaginous fishes, I found that cerebellum complexity was

positively associated with complexity in habitat, social behavior, depth of habitat and

migration. I also found results suggesting that parental care, change of medium and sexual

selection could be affecting cerebellum size. Among fishes held and bred in captivity, the

pattern was similar with an increased cerebellar complexity associated with complexity in

holding environment (Table 1).

My results on birds suggest that there is a positive association between cerebellum

complexity and complexity in nest- and bower building, habitat complexity, cognitive

abilities, mating system and altricial or semialtricial maturation (Table 1). In polygynous

species and precocial species the pattern was reversed and these factors correlated with a less

complex cerebellum. Species with a very shifting diet, or who capture prey or who has to

change location to forage, i.e. from air to ground or reverse, tended to have a more complex

cerebellum than those with a non-shifting diet or that forage in their primary habitat.

As mentioned earlier I did not find any analyses of the link between ecology or behavior

and cerebellum morphology in mammals. Exclusively for the mammals, there was a positive

association between cerebellum and language and memory in humans, and increased pain

thresholds after cerebellar-lesion in primates and carnivores (Table 1). In mammals and birds,

tool use correlated positively with a more complex cerebellum. However, proto tool use was

not significantly associated with cerebellum size or foliation. The pattern of social behavior as

2014

Ethology 9

a driver of an enlarged cerebellum was similar in mammals, cartilaginous- and bony fishes

and birds (Table 1). A positive association between echo localization and infrasound

producing was found in three mammalian groups (Table 1).

Change of medium seems to require an enlarged cerebellum since there was a positive

correlation between cerebellum size and the occurrence of changing of medium in both

mudfishes and birds (Table 1). Moreover, movements in the vertical direction correlated

positively with complexity in cerebellum across taxa (Table 1). It seems to be crucial how

deep an animal can dive to forage, since the deep divers had larger cerebellum than the

shallow divers, in both ducks and cichlid fishes. A similar pattern was seen in cartilaginous

fishes. Deep diving sharks had larger cerebellum than shallow divers, but in holocephalans the

ratio was the opposite, with a smaller cerebellum in the deep divers. Among cichlid fishes

there was also a difference between sexes, with males living in deeper habitats having larger

cerebellum than females living in deeper habitats. Wide-range movements in a horizontal

direction, migrations, were also positively associated with a complex cerebellum in

cartilaginous- and bony fishes, but in birds no significant correlation was found between the

occurrence of migration and cerebellum morphology (Table 1). This could be due to the few

migratory species used in the study (Bennett & Harvey, 1985).

Sharks with lesion of the cerebellar nuclei failed to coordinate the swimming movements,

and failed to swim in a straight line (Table 1). The motor ability in sharks with lesion of the

cerebellar corpus was not affected, but in birds the motor ability decreased. In bony fishes

and mammals cerebellar-lesion had no effect in low speed movement, but in bony fishes high

speed movement decreased (Table 1). Cerebellar-lesion in both bony fishes and mammals

resulted in i) decreased anxiety-like behavior and ii) a negative effect on a task of classical

conditioning. I found demonstrations of a positive association between cerebellum and

different learning abilities in all taxa, except cartilaginous fishes and amphibians (Table 1).

Visual and auditory discrimination learning failed after cerebellar-lesion in reptiles, birds and

mammals. In birds there was also a negative effect on operant conditioning following

cerebellar-lesion.

Among bony fishes, motor activity could both increase and decrease with larger

cerebellum size, depending on environment (Table 1). In guppies, females had larger

cerebellum than males and were more active (Table 1). Salmonids held in captivity became

2014

Ethology 10

more active and developed a less complex cerebellum in non-complex environment (Table 1).

The cognitive ability and learning in spatial tasks failed or decreased followed cerebellar-

lesion in bony fishes, birds and mammals, and in mammals also in 3-dimensional spatial

tasks.

The cerebellum was involved in electroreception among water living animals from

different taxa: lampreys, cartilaginous- and bony fishes, amphibians and mammals (Meek et

al. 2008; Rose, 2004). One mammalian species (echidna) were terrestrial though (Meek et al.

2008).

In the class lampreys I found no data on cerebellum morphology linked to ecology,

behavior or locomotion. Among the cartilaginous fishes, I did not find reports on cerebellum

morphology linked to specific behaviors. This is probably due to that relatively little is still

known about the behavior in cartilaginous fishes (Yopak et al. 2007; Lisney et al. 2008).

Surprisingly, I did not found any report of cerebellum morphology associated to ecology

among mammals.

2014

Ethology 11

Table 1. Overview of cerebellum functions. Vertebrate class (Class), number of species, if the study has taken phylogenetic relationships (Phylo. cont.) into account, which cerebellar variable (CB-data) that has been used, which factor the CB-data is linked to, the response (Resp.). Size = as a proportion of the total brain size, Ec = ecology, Be = behavior, Fu = function, Lo = locomotion, Ref = reference. (1) One non-extinct species.Refernces: 1; Yopak et al. 2007, 2; Yopak & Montgomery, 2008, 3; Yopak & Frank, 2009, 4; Lisney et al. 2008, 5; ten Cate, 1930 in New, 2001, 6; Karamyan, 1962 in New, 2001, 7; Kotrschal et al. 2012, 8; Kihslinger & Nevitt, 2006, 9; Gonda et al. 2011, 10; Pollen et al. 2007, 11; Kotrschal et al. 2012, 12; Kolm et al. 2009, 13; Gonzalez-Voyer & Kolm, 2010, 14; Rodríguez et al. 2005, 15;Roberts et al. 1992, 16; Rose, 2004, 17; Watson, 1978, 18; Cadwallader, 1974, 19; Iwaniuk et al. 2009, 20; Iwaniuk et al. 2006, 2007, 21; Hall et al. 2013, 22; Walsh et al. 2013, 23; Bennett & Harvey, 1985, 24; Iwaniuk et al. 2007, 25; Iwaniuk et al. 2006, 26; Day et al. 2005, 27; Kalisinska, 2005, 28; Monjan & Peters, 1970, 29; Spence et al. 2009, 30; Bobée et al. 2000, 31; Joyal et al. 1996, 32; Gandhi et al. 1999, 33; Ryding et al. 1993, 34; Peterson & Fiez, 1993, 35; Botez, 1992, 36; Grafman et al. 1992; Appollonio et al. 1993; Pascual-Leone et al. (in press), in Leiner et al. 1993, 37; Ivry & Baldo, 1992, in Leiner et al. 1993, 38; Wallesch & Horn, 1990, 39; Lewis & Barton, 2004, 40; Paulin, 1993 41; Davis et al. 1970, 42; Obayashi et al. 2001, 43; Watson & McElligott, 1984; 44; Yeo et al. 1985, 45; Buchtel, 1970, 46; Cantalupo & Hopkins, 2010, 47; Andersson, 1993, 48; Bshary et al. 2014, 49; Maseko et al. 2012, 50; Andreasen, et al. 1999, 51; Taylor et al. 1995. 52; Leggio et al. 2000, 53; Barash et al. 1999, 54; Desmond, et al. 1997, 55; Huang & Ricklefs, 2013, 56; Leiner et al. 1986, 57; MacLeod et al. 2003.

Class # Species Study Phylo. cont. Group CB-data Factor Resp Ec Be Fu Lo RefPetromyzontida,

Lampreys 1 species 1 No Neural circuits Electroreception + * 16

Chondrichthyans, cartilaginous fishes

Holocephalii2 species, 2 families 2 Yes A Size Habitat complexity - * 1

Prey movement speed - *Swimming speed - *

Foliation Habitat complexity + *Prey movement speed + *Swimming speed + *

Elasmobranchii, sharks, 43 species,

20 familiesYes B

Size Habitat complexity + *Prey movement speed + *Swimming speed + *Activity + *Migration + *Sociality + *

Foliation Habitat complexity + *Prey movement speed + *Swimming speed + *Activity + *Migration + *Sociality + *

C Size Habitat complexity - *Prey movement speed - *Swimming speed -

Foliation Habitat complexity + *Prey movement speed + *Swimming speed + *

2014

Ethology 12

Class # Species Study Phylo. cont. Group CB-data Factor Resp Ec Be Fu Lo RefD Size Habitat complexity - *

Prey movement speed - *

Swimming speed - *Activity - *

Sociality - *Foliation Habitat complexity + *

Prey movement speed + *Swimming speed + *

Activity + *Sociality + *

E Size Habitat complexity + *Prey movement speed + *

Swimming speed + *Foliation Habitat complexity + *

Prey movement speed + *Swimming speed + *

Holocephalii7 species, 3 families 3 Yes A Size Depth - * 2

Prey movement speed - *Swimming speed - *

Foliation Depth - *Prey movement speed + *Swimming speed + *

B Size Depth - *Prey movement speed - *Swimming speed - *

Foliation Depth - *Prey movement speed + *Swimming speed + *

Elasmobranchii, sharks

15 species, 8 familiesYes C

Size Depth + *Prey movement speed - *Swimming speed - *

Foliation Depth - *Prey movement speed + *Swimming speed + *

2014

Ethology 13

Class # Species Study Phylo. cont. Group CB-data Factor Resp Ec Be Fu Lo RefD Size Depth + *

Prey movement speed + *Swimming speed + *

Foliation Depth + *Prey movement speed + *Swimming speed + *

Elasmobranchii, sharks, 1 species 4 Yes

Size Habitat complexity + * 3Depth + *Diet: filter feeder + *Migration + *Swimming speed - *

Foliation Habitat complexity + *Depth + *Diet: filter feeder + *Migration + *Swimming speed - *

Elasmobranchii, batoids

24 species, 8 families5 Yes A

Size Habitat complexity - * 4

Swimming speed - *Foliation Habitat complexity + *

Swimming speed + *B Size Habitat complexity + *

Swimming speed +Foliation Habitat complexity + *

Swimming speed + *Elasmobranchii, sharks, 1 species

6 No Lesionnuclei

Coordinated swimmingStraight line swimming

- * 5, 6

Lesioncorpus

Motor ability No effect *

Batoids, skates1 species 7 No

Lesioncorpus

and nucleiMotor activity + * 6

Elasmobranchii, Holocephalii,

4 speciesNo

Neural circuits Electroreception + * 16

Osteichthyes,bony fishes

Cyprinodontiformes1 species

8 No Size Female activity + * * 7

2014

Ethology 14

Class # Species Study Phylo. cont. Group CB-data Factor Resp Ec Be Fu Lo RefSalmoniformes

1 species 9 No A Size Habitat complexityRiver + * 8

B Captivity environment, + *Activity - *

Gasterosteiformes1 species 10 No A Size Habitat, wild-caught + * 9

B Habitat, captivity - *Perciformes

7 species, 1 family 11 No Size Habitat complexity + * 10

Number of species in habitat + *Salmoniformes

1 species 12 No A Size Wild-type + * 11

B Transgenic - *C Transgenic, environment stream - *D Transgenic, environment hatchery + *

Salmoniformes1 species 13 No Size Migration + * 12

Perciformes43 species, 1 family 14 Yes Size Habitat complexity + * 13

Depth + *Sexual selection - *Care type: biparental or female - *Depth (female) - *Depth (male) + *Care type (male) - *

Cypriniformes1 species

15 No Lesion Classical conditioning, motor reflexes.Emotional learning.Spatial cognition.

- * 14

Salmoniformes1 species 16 No Lesion Low speed swim No effect * 15

High speed swim - *Mormyriformes

1 species Gymnotiformes

1 species

17 No

Neural circuits Electroreception + * 16

Salmoniformes1 species 18 No Lesion Discrimination learning - * 17

Protopteri, Mudfishes 19 No Size Change of medium + * 18Burrowing + *

2014

Ethology 15

Class # Species Study Phylo. cont. Group CB-data Factor Resp Ec Be Fu Lo Ref

Teleosts No Neural circuits Sociality + * 48

Amphibia,amphibians

Salamander, 1 species Caecilians, 1 species 20 No Neural

circuits Electroreception + * 16

Anura, 6 species No Size Habitat complexity + * 51

Reptilia,reptiles

Squamata, 1species Testudines, 1 species 21 No Lesion Discrimination learning - * 17

Aves,birds

96 species, 42 families

22 Yes Size Cognition + * 19Foliation Cognition + *

107 species 23 Yes Size Tool use ns * 20Foliation Tool use + *

Size Proto-tool use ns *Foliation Proto-tool use ns *

64 species 24 Yes Foliation Complexity in nest construction + * 2160 extinct species(1) 25 No Flocculus Evolution of flying ability no * 22

139 species, 54 families, 21 orders 26 No Size Habitat complexity + * 23

Migration ns *Diet: varying and/or capture prey + *Foraging: change of medium + *Mating system: monogamous + *Maturation: altricial or semialtricial + *

96 species, 42 families, 21 orders 27 Yes Folia size

(I-X) Strong hindlimbs + anterior lobe size * 24

Strong fliers - I-V+ VI-VII *

91 species, 41 families, 21 orders 28 No Foliation Maturation: altricial + * 25

Maturation: precocial - *Passeriformes,

5 species 29 Yes Size Complexity in bower construction + * 26

10 species,2 subfamilies 30 No Size Foraging: diving depth + * 27

Columbiformes,1 species 31 No Lesion Recognition memory.

Operant conditioning. - * 28

Passeriformes,1 species 32 No Lesion Spatial cognition - * 29

Motor ability - *

2014

Ethology 16

Class # Species Study Phylo. cont. Group CB-data Factor Resp Ec Be Fu Lo Ref

Mammalia,mammals Rodents, 1 species 33 No Lesion

Attention abilities, reaction to noise.Anxiety-like behavior.Interest in known area.

- * 30

Motor activity.Burying, electric shock from electrode.Interest in unknown area.

+ *

Rodents, 1 species 34 No Lesion Spatial learning. - * 31Bridge/beam, balance.Grid, climbing - *

Rodents, 1 species 35 No LesionLatency in Morris water-maze task.Time spent in target quadrant.Motor activity.

+ * * 32

Swimming speed No effect *

Primates, 1 species 36 No Neural activity Mental imagery + * 33

Primates, 1 species 37 No Neural activity Word-processing + * 34

Lesion Non-motor learning and error-detection - *

Primates, 1 species 38 No Lesion Visuo-spatial organization in:Cognitive planning and info. processing. - * 35

Primates, 1 species 39 No AtrophyCognitive planning.Word-retrieval.Procedural learning.

- * 36

Primates, 1 species 40 No Atrophy or lesion

Verbal associative learning.Judging time intervals, velocity of moving stimuli.

- * 37

Primates, 1 species 41 No Lesion Spatial cognition in 3-D environment - * 38Monotremes,

2 species 42 No Neural circuits Electroreception + * 16

Primates, 14 species 43 Yes Size Social play + * 39Monotremes,

Marine mammals,Microchiropterans

44 No Neural circuits

Spatial orientation and navigation.Prey detection.Communication.

+ * * * 40

Carnivora, 1 species 45 No Lesion Discrimination learning - * 41

Primates, 1 species 46 No Neural circuits Tool use + * 42

Rodent, 1 species 47 NoChemical

mani-pulation

Motor learning + * 43

Rodent, 1 species 48 No Lesion Classical conditioning - * 44

2014

Ethology 17

Class # Species Study Phylo. cont. Group CB-data Factor Resp Ec Be Fu Lo RefRodent, 1 species 49 No Lesion Discrimination learning - * 45

Primates, 3 species 50 No Size Tool use + * 46Primates, 2 species 51 No Size Throwing + * 46Rodents, 1 species 52 No Size Attention abilities + * 47Primates, 1 species Carnivora, 1 species 53 No Lesion Pain thresholds + * 17

Odontocete cetaceans,Microchiroptera 54 No Neural

circuits Echolocation + * 49

Elephantidae,3 species 55 No Neural

circuits Infrasound + *

Primates, 1 species 56 No Neural circuits Episodic memory + * 50

Primates, 1 species 57 No Neural circuits Working memory + * 54

Rodent, 1 species 58 No Lesion Spatial learning by observation - * 52Primates, 1 species 59 No Lesion Saccadic eye movement - * 53

Primates, 1 species 60 No Neural circuits

Active perceptionProcedural learningSociality

+ * * 55

Primates, 1 species 61 No Neural circuits Cognition + * 56

Primates, 16 species 62 No Size

Visual-spatial skills.Planning of complex movements.Procedural learning.Attention switching.Sensory discrimination.

+ * * 57

2014

Ethology 18

Discussion My literature study shows that the cerebellum is important for several advanced behavior

sequences and that it plays a key role during adaptation to more complex environments.

Below I list the main factors that were associated with variation in cerebellum size and

complexity.

Evolutionary age in phylogeny

At the large scale level my results imply that a more complex cerebellum is associated

with derived species of relatively young evolutionary age. This was the case in cartilaginous

fishes, bony fishes and birds (Yopak et al. 2007; Lisney et al. 2008; Pollen et al. 2007;

Gonzales-Voyer & Kolm, 2010; Hall et al. 2013). The species within these taxa, which was

associated with a complex cerebellum, were not necessarily close related to each other.

Evolutionary young species often has to occupy new habitats in the environment, which may

lead to species highly specialized to a specific niche. Adaptations to a specific niche may

require advancement in behavior. The effect in cerebellum complexity as a consequence of

evolutionary age is generally difficult to separate from the effect of habitat complexity.

Consequently, the morphological variation seen in the brain structure cerebellum cannot be

fully explained by phylogenetic relationships. Instead, ecological and behavioral factors play

a major role in the neural role of cerebellum.

Habitat complexity

One ecological factor in particular seems to be strongly correlated with a more complex

cerebellum. Species that live in 3-dimensional (i.e. oceanic habitat or coral reefs in aquatic

environments, or the airspace or arboreal habitats in terrestrial environment), and therefore

most likely a complex environment, have a more complex cerebellum than species living in a

2-dimensional environment (i.e. benthic or demersal habitats in aquatic environment, or

grassland or habitat near the ground in terrestrial environment). A 3-dimensional environment

necessitates multidirectional navigation and orientation capacities in both a horizontal and a

vertical direction, and also enables a more complex pattern of movements and enhanced

motor coordination, as compared to a 2-dimensional habitat, where only horizontal navigation

is needed. This pattern has been observed in cartilaginous fishes, amphibians and birds,

suggesting it is a common characteristic among vertebrates.

2014

Ethology 19

The relative size of the cerebellum in elephants is the largest among all mammals, and the

cerebellum is also highly foliated in the elephant. A large cerebellum is also found among

Odontocete cetaceans, toothed whales and echo locating bats (microchiroptera) (Maseko et al.

2012). The cerebellum plays a major role in motor control (Butler & Hodos 2005; Kandel et

al. 2013; Thach et al. 1992), and all these three groups have very specialized motor abilities

that have not been observed among the majority of other mammals: swimming in whales,

flying in bats and use of the unusual trunk in elephants. At the same time, both cetaceans and

microchiropterans have adapted to a 3- dimensional lifestyle, cetaceans to an aquatic

environment and microchiropterans to an aerial environment (Maseko et al. 2012).

Presumable there is an association between habitat complexity and cerebellum complexity in

mammals.

One interesting result was the association between changing of medium and complexity

in cerebellum in both mudfishes and birds (Table 1). To change medium an animal has to

change its movement patterns quite dramatically, i.e. from flying to swimming in birds and

from swimming to burrowing in mudfishes (Bennett & Harvey, 1985; Cadwallader, 1974). As

mentioned previously, the major role of cerebellum is coordination of movements (Butler &

Hodos, 2005). Hence, to have a wide repertoire of movements and the ability to change

locomotion seems to require a complex cerebellum. Another property when changing medium

is the often broad changes in behavior that occur (Cadwallader, 1974).

With an increased complexity in environment a necessity of enhancement in coordination

of movements may follow, since one of the major roles of cerebellum is motor control (Butler

& Hodos, 2005), an enlarged cerebellum can evolve in these habitats. But complex

environments also require higher cognitive and learning abilities than non-complex

environment, due to the intra- and inter specific interaction pressure (Pollen et al. 2007), and

my results imply that the cerebellum plays a role for these abilities too (Table 1).

Vertical and horizontal movements and migrations

Migratory species require good orientation and navigation abilities to perform these

movements over great distances. Several lesion studies in bony fishes, birds and mammals

indicate that the spatial cognition ability decreases following cerebellar-lesion (Table 1), and

therefore it is reasonable to suppose that the cerebellum has a major role in migration across

vertebrate classes. Among the cartilaginous fishes, the migratory species have a more

2014

Ethology 20

complex cerebellum than non-migratory species (Yopak & Frank, 2009; Yopak &

Montgomery, 2008). The relatively largest and most foliated cerebellum among cartilaginous

fishes is found in one species that migrate up to one mile in the vertical direction (Yopak &

Frank, 2009). Even within species there is substantial variation in cerebellar size depending

on lifestyle. Migratory brown trout (Salmo trutta) has a relatively larger cerebellum than non-

migratory individuals (Kolm et al. 2009). This strengthens the supposition that the cerebellum

is crucial for orientation and navigation.

Interestingly, I did not find any studies of the link between ecological variables and

cerebellum morphology among mammals. As mentioned previously, elephants and whales

have the largest (also when controlling for body size) cerebellum among mammals and their

cerebellum is also highly foliated (Maseko et al. 2012). Moreover elephants and whales are

also known to be extremely wide-range moving animals (Wittemyer et al. 2007), which

indicate that the positive association in migration and cerebellar complexity could be similar

in mammals as in other taxa.

Among both elasmobranchii and bony fishes there was a tendency that increasing habitat

depth is associated with a more complex cerebellum (Yopak & Montgomery, 2008; Yopak &

Frank, 2009; Gonzales-Voyer & Kolm, 2010). Intriguingly, in the holocephalans this pattern

was reversed (Yopak & Montgomery, 2008), which could be explained by these species living

in depths where conspecifics are scarce, the temperature is low which leads to low swimming

speed and low overall activity levels (Yopak & Montgomery, 2008).

In ducks, a positive association between increasing diving depth and cerebellar

complexity was reported (Kalisińska, 2005). Among birds that have to change location from

ground to air or from air to ground to forage, there was also an association between vertical

movements and the complexity of cerebellum reported (Bennett & Harvey, 1985). Like in

horizontal migrations it seems like vertical movements require good orientation ability and

therefore these species evolve a more complex cerebellum.

In guppies, there was a positive association between cerebellum size and females.

Kotrschal et al. (2012) argues that this is due to the guppy lifestyle, were females often got

chased by males and therefore require more time foraging.

2014

Ethology 21

Complex coordinated behaviors

Elephants, cetaceans and microchiropterans have unusual and specialized vocalization

systems, infrasound in elephants and echolocation in cetaceans and microchiropterans

(Maseko et al. 2012). The infrasound in elephants is produced by the elephant trunk, which is

a highly specialized part of the body, consisting of a complex muscle pattern (Endo et al.

2001). The echolocation in bats is produced both by flapping flight and laryngeal vocalization

(Speakman, 2001), while in cetaceans echolocalization is produced by a complex air sac

within the blowhole (Reidenberg &Laitman, 2008). Maseko et al. (2012) argues that the

producing of these sounds, highly muscular control is needed, and therefore an enlarged

cerebellum could have evolved in these three mammalian groups.

To perform behaviors such as nest building and bower building in birds, high processing

capacity, procedural learning and motor planning is required, which have been associated

positively with the cerebellum (Hall et al. 2013; Day et al. 2005). In bowerbirds, the enhanced

cerebellum seems to have evolved due to sexual selection and female choice, since females

choose to mate with males with the most decorated and most complex designed bowers (Day

et al. 2005). Day et al. (2005) also argued that the bower building also was dependent on

context learning. Context learning is dependent of ability to associating a particular context

with a particular motor sequence (Thach, 1996), which is needed in both nest- and bower

building. However, if there is a sexual dimorphism in cerebellum size in bower birds or birds

with complex nests is still unclear.

The occurrence of tool use in birds and primates and throwing objects in primates was

associated with a larger and more complex cerebellum in these taxa (Table 1). In birds, a

higher cerebellar foliation degree has also been demonstrated to be positively associated with

tool use (Iwaniuk et al. 2009). To use a tool or throw an object requires motor planning and

also often learning. Cerebellum size correlates with these two behaviors, which suggests that

the cerebellum is involved in diverse functions that require higher mental skills (Iwaniuk et al.

2009). Accordingly, the mechanism to perform complex coordinated behavior seems to be at

the neural level.

The floccular fossa was thought to be the origin of flying ability in early birds, because of

its gaze stabilization function when rotating the head. To stabilize the gaze is a presumption

for the ability to fly. No significant correlation was found between floccular fossa size and

2014

Ethology 22

evolution of flying ability in this study (Walsh et al. 2013). Iwaniuk et al. (2007) found an

association between small size of folia I-V, and large size of folia VI-VII in strong fliers, and

a positive correlation between anterior lobe size and strong hind limbs, which suggest that

different parts of the cerebellum has different roles in locomotion. Hence, there is certainly

room for improvement in our understanding of how fine-scale variation in cerebellum

structures may affect behavior.

Complex cognitive behaviors

Cerebellum has an important role for social behavior and this pattern was similar across

taxa (Table 1). In cartilaginous- and bony fishes, birds and mammals, a larger cerebellum was

associated with increased sociality, at both the intra- and interspecific level (Striedter, 2005;

Yopak et al. 2007; Bshary et al. 2014; Gonzales-Voyer & Kolm, 2010; Bennett & Harvey,

1985; Pollen et al. 2007). Social behavior requires advanced cognitive abilities (Dunbar,

1998), and we also find a more complex cerebellum across highly social taxa (Iwaniuk et al.

2009; Kotrschal et al. 2012; Pollen et al. 2007).

Previously the cerebellum was thought to be limited to only have a role in motor learning

(Lalonde & Botez, 1990; Thach et al. 1992), but several studies have shown that the

cerebellum is also involved in learning that does not involve movements, such as classical-

and operant conditioning, spatial learning, recognition, visual and auditory discrimination

learning (Table 1). This suggests that the cerebellum is not only involved in learning required

for muscle and movements control, but also plays a role for cognitive behaviors and mental

skills.

The cerebellum seems to be involved in emotions. Cerebellar-lesions have been shown a

decreased pattern of fear and anxiety in behavioral tests across taxa (Table 1). Fear and

anxiety is often referred to as shyness (Wilson et al. 1994), which might imply that

cerebellum at least partially could be involved in personality.

The cerebellum seems to be involved in spatial cognition across taxa (Table 1). The

hyperactivity following a fatigue environment and/or cerebellar-lesion could be a causation of

the animal being stressed when not being able to orient in this environment. This has been

seen in cartilaginous fishes and mammals (Table 1).

2014

Ethology 23

Electroreception

The cerebellum plays a role in electroreception among lampreys, cartilaginous- and bony

fishes and mammals (Meek et al. 2008; Rose, 2004). Species with electroreception perception

abilities are often distantly related. Hence, electroreception has developed convergent at

different times during the evolution (Rose, 2004; Bullock, 1999; Paulin, 1993). Interestingly,

the relatively largest and most foliated cerebellum among vertebrates is found in -the

mormyrid fishes (Butler & Hodos, 2005). There are two ways in which an animal can utilize

electric fields, either to detect preys, or to generate electric fields themselves for

communication and spatial mapping (Paulin, 1993). The mormyrid fishes are able to both

generate- and to sense externally generated electric fields. It is believed that the control

system for the mormyrid fishes electroreception requires an enormous cerebellum (Butler and

Hodos, 2005; Rose, 2004; Striedter, 2005). The cerebellum is therefore not only a center for

control of movements of the animals themselves, but also a key brain structure in the

perception and detection of external movements in the environment (Paulin, 1993).

Conclusion

My review of existing literature in cerebellum morphology and function across

vertebrates supports the hypothesis that the cerebellum is of great importance for a wide

variety of functions across taxa, and that there are certain similar patterns of ecological forces

driven the evolution of cerebellum variation. There is a strong association between a large or

complex cerebellum and complex behavior sequences, or a variable and shifting ecology. This

is partially dependent on phylogenetic relationships. Complexity of the cerebellum is often

found in unrelated species that share certain lifestyle characteristic, such as habitat

complexity, diet, migration, changing of medium or species that share certain behavior

characteristic, such as the construction of complex nests or bowers in birds, tool use in birds

and primates, or even complex cognitive abilities in birds and mammals.

For an adequate and complete picture of the function of cerebellum in vertebrates we still

lack certain data, especially from artificial selection experiments at all taxonomical levels.

Moreover, lampreys, amphibians and reptiles are underrepresented in all perspectives. We

also lack data from a behavioral and functional view in cartilaginous fishes, and concerning

the ecological factors that correlate with a larger and/or more foliated cerebellum in

mammals. The link between cerebellum morphology in relation to social behavior, learning

2014

Ethology 24

and cognition is still largely unknown among vertebrates. Further research is thus needed to

fully understand the interesting non-motor function of cerebellum.

AcknowledgementI wish to thank course leader Cilla Kullberg for your useful advice and Johan Lind for

giving me perceptive feedback and perspective. I wish to thank my sponsors Birger and Ulla

Johansson for your generous support. Last but not least, I wish to thank my excellent

supervisor Niclas Kolm, whose knowledge and advice have been of great value for this

project. I am grateful for your enthusiasm, patience and helpful support.

ReferencesAndersson, B. (1994) The volume of the cerebellar molecular layer predicts attention to

novely in rats. Brain Research 641: 160-162.Andreasen, N. C., O´Leary, D. C., Paradiso, S., Cizadlo, T., Arndt, S., Watkins, G. L., Boles

Ponto, L., Hichwa, R. D. (1999) The cerebellum plays a role in conscious episodic memory retrieval. Human Brain Mapping 8: 226-234.

Appollonio, I. M., Grafman, J., Schwarts, V., Massaquoi, S., Hallett, M. (1993) Neurology 43: 1536-1544 in Leiner, H. C., Leiner, A. L., Dow, R. S. (1993) Cognitive and language functions of the human cerebellum. TINS 16: 444-447.

Barash, S., Melikyan, A., Sivakov, A., Zhang, M., Glickstein, M., Thier, P. (1999) Saccadic dysmetria and adaptaion after lesions of the cerebellar cortex. J. Neurosci. 19: 10931-10939.

Bshary, R., Gingins, S., Vail, A. L. (in press) Social cognition in fishes. Trends in Cognitive Sciences.

Barnard, C. (2003) Animal Behaviour: Mechanism, Development, Function and Evolution. Pearson, Prentice Hall.

Barton, R. A. (2012) Embodied cognitive evolution and the cerebellum. Phil. Trans. Soc. B 367: 2097-2107.Bennett, P. M. & Harvey, P. H. (1985) Relative brain size and ecology in birds. J. Zool. Lond. 207:151-169.

Bobèe, S., Mariette, E., Tremblay-Leveau, H., Caston, J. (2000) Effects of early midline cerebellar lesion on cognitive and emotional functions in the rat. Behavioural Brain Research 112: 107-117.

Boogert, N. J., Anderson, R. C., Peters, S., Searcy, W. A., Nowicki, S. (2011) Song repertoire in male song sparrows correlates with detour reaching, but not with other cognitive measures. Animal Behaviour 81: 1209-1216.

Botez, M. I. (1992) The neuropsychology of the cerebellum: an emerging concept. Arch. Neurol. 49: 1229-1230.

Bracke-Tolkmitt, R et al. (1989) Behav. Neurosci. 103: 442-446. In Leiner, H. C., Leiner, A. L., Dow, R. S. (1993) Cognitive and language functions of the human cerebellum. TINS 16: 444-447.

2014

Ethology 25

Buchtel, H. A. (1970) Visual-learning deficits following cerebellar damage in rats. J. Comp. Physiol. Psychol. 72: 296-305.

Bullock, T. H. (1999) The future of research on electroreception and electrocommunication. The J. of Experimental Biol. 202: 1455-1458.

Butler, A. B. & Hodos, W. (2005) Comparative Vertebrate Neuroanatomy: Evolution and Adaptation. Wiley, 2nd ed.

Cadwallader, P. L. (1974) Relationship between brain morphology and ecology in New Zealand Galaxiidae, particularly Galaxias vulgaris (Pisces: Salmoniformes). New Zealand J. of Zool. 2: 35-43.

Davis, H. N., Watkins, G. M., Angermeier, W. F., Rubia, F. J. (1970) The role of cortial parts of the cerebellar hemispheres in discrimination learning in cats. Plügers Archiv. Ges. Physiol. Men. Tier. 318: 346-352.

Day, L. B., Westcott, D. A., Olster, D. H. (2005) Evolution of Bower Complexity and Cerebellum Size in Bowerbirds. Brain Behav. Evol. 66: 62-72.

Desmond, J. E., Gabrieli, J. D. E., Wagner, A. D., Ginier, B. L., Glover, G. H. (1997) Lobular patters of cerebellar activation in verbal working memory and finger-tapping tasks as revealed by functional MRI. J. Neurosci. 17: 9675-9685.

Dunbar, R. M. I. & Shultz S. (2007) Evolution in the social brain. Science 317: 1344-1347.Dunbar, R. I. M. (1998) The Social Brain Hypothesis. Evolutionary Anthropology, 178-190. Endo, H., Hayashi, Y., Komiya, T., Narushima, E., Sasaki, M. (2001) Muscle architecture of

the elongated nose in the Asian elephant (Elephas maximus). J. Vet. Med. Sci. 63: 533-537.

Falconer, D. S. & Mackay, T. F. C. (1996) Introduction to Quantitative Gentetics. Longmans Green, 4th ed.

Gandhi, C. C., Kelly, R. M., Wiley, R. G., Walsh, T. J. (2000) Impaired acquisition of a Morris water maze task following selective destruction of cerebellar purkinje cells with OX7-saporin. Behavioural Brain Research 109: 37-47.

Gonda, A., Herczeg, G., Merilä, J. (2011) Population variation in brain size of nine-spined sticklebacks (Pungitius pungitius) – local adaptation or environmentally induced variation? Evol. Biol. 11: 1471-2148.

Gonzales-Voyer, A., Kolm, N. (2010) Sex, Ecology and the Brain: Evolutionary Correlates of Brain Structure Volumes in Tanganyikan Cichlids. In press PLoS ONE.

Grafman, J. et al. (1992) Neurology 42: 1493-1496 in Leiner, H. C., Leiner, A. L., Dow, R. S. (1993) Cognitive and language functions of the human cerebellum. TINS 16: 444-447.

Hall, Z. J., Street, S. E., Healy, S. D. (2013) The evolution of cerebellum structure correlates with nest complexity. Biol. Lett. 9: 20130687.

Healy, S. D., Haggis, O., Clayton, N. S. (2010) Zebra Finches and Cognition. Emu 110: 242-250.

Hickman, C. P., Roberts, L. S., Keen, S. L., Larson, A., Eisenhour, D. J. (2012) Animal Diversity. The Mc-Graw-Hill Companies, 6th ed.

Huang, C. & Ricklefs, R. E. (2013) Cerebellum and Human Evolution: A Comparative and Information Theory Perspective, in Handbook of the Cerebellum and Cerebellar Disorders. Springer Netherlands pp 1337-1357

2014

Ethology 26

Ivry, R. B. & Baldo, J. U. (1992) Curr. Opin. Neurobiol. 2: 212-216, in Leiner, H. C., Leiner, A. L., Dow, R. S. (1993) Cognitive and language functions of the human cerebellum. TINS 16: 444-447.

Iwaniuk, A. N., Hurd, P. L., Wylie, D. R. W. (2006) Comparative Morphology of the Avian Cerebellum: I. Degree of Foliation. Brain Behav. Evol. 68: 45-62.

Iwaniuk, A. N., Hurd, P. L., Wylie, D. R. W. (2007) Comparative Morphology of the Avian Cerebellum: II. Size of Folia. Brain Behav. Evol. 69: 196-219.

Iwaniuk, A. N., Wylie, D. R., Lefebvre, L. (2009) The Comparative Approach and Brain-Behaviour Relationships: A Tool for Understanding Tool Use. Canadian Journal of Experimental Psychology 63:150-159.

Jerison, H. J. (1973) Evolution of the Brain and Intelligence. New York: Academic Press.Joyal, C. C., Meyer, C., Jacquart, G., Mahler, P., Caston, J., Lalonde, R. (1996) Effects of

midline and lateral cerebellar lesions on motor coordination and spatial orientation. Brain Research 739: 1-11.

Kalisińska, E. (2005) Anseriform Brain and Its Parts versus Taxonomic and Ecological Categories. Brain Behav. Evol. 65: 244-261.

Kandel, E. R., Schwartz, J. H., Jessell, T. M., Siegelbaum, S. A., Hudspeth, A. J. (2013) Principles of Neural Science. The McGraw-Hill Companies, 5th ed.

Karamyan, A. I. (1962) Evolution of the function of the cerebellum and cerebral hemispheres in New J. G. (2001) Comparative neurobiology of the elasmobranch cerebellum: theme variation on a sensorimotor interface. Environmental Biology of Fishes 60: 93-108.

Kihslinger, R. L. & Nevitt, G. A. (2005) Early rearing environment impacts cerebellar growth in juvenile salmon. The journal of experimental biology 209: 504-509.

Kolm, N., Gonzales-Voyer, A., Brelin, D., Winberg, S. (2009) Evidence for small scale variation in the vertebrate brain: mating strategy and sex affect brain size and structure in wild brown trout (Salmo trutto). J. Evol. Biol. Doi: 10.1111/j.1420-9101.2009.01875.x

Kotrschal, A., Rogell, B., Maklavakov, A. A., Kolm, N. (2012) Sex-specific plasticity in brain morphology depends on social environment of the guppy, Poecilia reticulate. Behav. Ecol. Sociobiol. DOI 10.1007/s00265-012-1403-7.

Kotrschal, A., Sundström, L. F., Brelin, D., Devlin, R. H., Kolm, N. (2012) Inside the heads of David and Goliath: environmental effects on brain morphology among wild and growth-enhanced coho salmon Oncorhynchus kisutch. Journal of Fish Biology 81: 987-1002.

Lalonde, R. & Botez, M. I. (1990) The cerebellum and learning in animals. Brain Research Reviews 15: 325-332.

Leggio, M. G., Molinari, M., Neri, P., Graziano, A., Mandolesi, L., Petrosini, L. (2000) Representation of actions in rats: The role of cerebellum inlearning spatial performances by observation. PNAS 97: 2320-2325.

Leiner, H. C., Leiner, A. L., Dow, R. S. (1986) Does the cerebellum contribute to mental skills? Behav. Neurosci. 100: 43-454.

Leiner, H. C., Leiner, A. L., Dow, R. S. (1993) Cognitive and language functions of the human cerebellum. TINS 16: 444-447.

Lewis, K. P. & Barton, R. A. (2004) Playing for keeps. Human Nature 15: 5-21.

2014

Ethology 27

Lisney, T. J., Yopak, K. E., Montgomery, J. C., Collin, S. P. (2008) Variation in Brain Organization and Cerebellar Foliation in Chondrichthyans: Batoids. Brain Behav. Evol. 72: 262-282.

MacLeod, C. E., Zilles, K., Schleicher, A., Rilling, J. K., Gibson, K. R. (2003) Expansion of the neocerebellum in Hominoidea. J. of Human Evol. 401: 401-429.

Maseko, C. B., Spocter, A. M., Haagensen, M., Manger, R. P. (2012) Elephants Have Relatively the Largest Cerebellum Size of Mammals. The anatomical record 295: 661-672.

Meek, J. (1992) Comparative Aspects of Cerbellar Organization. From Mormyrids to Mammals. European Journal of Morphology 30: 37-51.

Meek, J., Yang, J. Y., Han, V. Z., Bell, C. C. (2008) Morphological Analyses of the Mormyrid Cerebellum Using Immunohistochemistry, With Emphasis on the Unusual Neuronal Organization of the Valvula. The Journal of Comparative Neurology 510: 396-421.

Monjan, A. A. & Peters, M. H. (1970) Cerebellar lesions and task difficulty in pigeons. J. Comp. Physiol. Psychol. 72: 171-176.

Obayashi, S., Suhara, T., Kawabe, K., Okauchi, T., Maeda, J., Akine, Y., Onoe, H., Iriki, A. (2001) Functional Brain Mapping of Monkey Tool Use. Neuro Image 14: 853-861.

Oliveira, R. F. (2013) Mind the fish: zebrafish as a model in cognitive neuroscience. Frontiers in neural circuits 7: 131.

Pascual-Leone, A. et al. in press, Ann. Neurol. In Leiner, H. C., Leiner, A. L., Dow, R. S. (1993) Cognitive and language functions of the human cerebellum. TINS 16: 444-447.

Paulin, M. G. (1993) The role of the Cerebellum in Motor Control and Perception. Brain Behav. Evol. 41: 39-40.

Peterson, S. E. & Fiez, J. A. (1993) Theprocessing of single wordsstudied with positron emission tomography. Annu. Rev. Neurosci. 16: 509-530.

Pollen, A. A., Dubberfuhl, A. P., Scace, J., Igulu, M. M., Renn, S. C. P., Shumway, C. A., Hofman, H. A. (2007) Environmental Complexity and Social Organization Sculpt the Brain in Lake Tanganyikan Cichlid Fish. Brain Behav. Evol. 70: 21-23.

Reidenberg, J. S. & Laitman, J. T. (2008) Sisters of the sinuses: cetaceans air sacs. Anat. Rec. 291: 1389-1396.

Roberts, B. L., Van Rossem, A., De Jager, S. (1992) The influence of cerebellar lesions on the swimming speed performance of the trout. J. exp. Biol. 167: 171-178.

Rodríguez F., Durán, E., Gómez, A., Ocaña, F. M., Álvarez, E., Jiménez-Moya, F., Broglio, C., Salas, C. (2005) Cognitive and emotional functions of the teleost fish cerebellum. Brain Research Bulletin 66: 365-370.

Rose, G. J. (2004) Insights into neural mechanisms and evolution of behavior from electric fish. Nature Reviews 5: 943.

Ryding, E., Decety, J., Sjöholm, H., Stenberg, G., Ingvar, D. H. (1993) The cerebellum participates in mental activity: tomographic measurements of regional cerebralblood flow. Cogn. Brain Res. 1: 94-99.

Shettleworth, S. J. (2010) Cognition, Evolution, and Behaviour.Oxford University Press, 2nd ed.

Striedter G. F. (2005) Principles of Brain Evolution. Sinauer Associates, Sunderland.

2014

Ethology 28

Speakman, J. R. (2001) The evolution of flight and echolaocation in bats: another leap in the dark. Mammal Rev. 31: 111-130.

Spence, R. D., Zhen, Y., White, S., Schlinger, B. A., Day, L. B. (2009) Recovery of motor and cognitive function after cerebellar lesion in a songbird – role of estrogens. European J. of Neurosci. 29: 12225-1234.

Taylor, G. M., Nol, E., Boire, D. (1995) Brain Regions and Encephalization in Anurans: Adaptation or Stability? Brain Behav. Evol. 45: 96-109.

ten Cate, J (1930) Contribution a la physiologie compare du cervelet. III. Le cervelet des plagiostomes. Archiv. need. physiol. de l´homme et des animaux 15: 479-528 in New J. G. (2001) Comparative neurobiology of the elasmobranch cerebellum: theme variation on a sensorimotor interface. Environmental Biology of Fishes 60: 93-108.

Thach, W. T., Goodkin, H. P., Keating, J. G. (1992) The Cerebellum and the Adaptive Coordination of Movements. Annu. Rev. Neurosci. 15: 403-442.

Thach, W. T. (1996) On the specific role of cerebellum in motor learning and cognition: clues from PET activation and lesion studies in man. Behav. and Brain Sciences 19: 411-433.

Wallesch, C. W. & Horn, A. (1990) Long term effects of cerebellar pathology on cognitive functions. Brain Cogn. 14: 19-25.

Walsh, S. A., Iwaniuk, A. N., Knoll, M. A., Bourdon, E., Barrett, P. M., Milner, A. C., Nudds, R. L., Abel, R. L., Dello Sterpaio, P. (2013) Avian Cerebellar Floccular Fossa Size Is Not a Proxy for Flying Ability in Birds. In press PLos ONE.

Watson, M. & McElligott, J. G. (1984) Cerebellar norepinephrine depletion and impaired acuisition of specific locomotor tasks in rats. Brain Research 296: 129-136.

Watson, P. J. (1978) Nonmotor functions of the cerebellum. Psychol. Bull. 85: 944-967.Wilson, D. S., Clark, A. B., Coleman, K., Dearstyne, T. (1994) Shyness and boldness in

humans and other animals. Trends in Ecology and Evolution. 9: 442-446.Wittemyer, G., Getz, W. M., Vollrath, F., Douglas-Hamilton, I. (2007) Social dominance,

seasonal movements, and spatial segregation in African elephants: a contributionto conservation behavior. Behav. Ecol. Sociobiol. 61: 1919-1931.

Yeo, C. H., Hardiman, M. J., Glickstein, M. (1985) Classical conditioning of the nictitating membrane response in the rabbit. I. Lesions of the cerebellar nuclei. Exp. Brain. Res. 60: 87-98.

Yopak, K. E., Lisney, T. J., Collin, S. P., Montgomery, J. C. (2007) Variation in Brain Organization and Cerebellar Foliation in Chondrichthyans: Sharks and Holocephalas. Brain Behav. Evol. 69: 280-300.

Yopak, K. E., Montgomery, J. C. (2008) Brain Organization and Specialization in Deep-Sea Chondrichtyans. Brain Behav. Evol. 71:287-304.

Yopak, K. E., Frank, L. R. (2009) Brain Size and Brain Organization of the Whale Shark, Rhinocodon typys, Using Magnetic Resonance Imaging. Brain Behav. Evol. 74: 121-142.

2014

Ethology 29

2014

Ethology 30

2014