Download Variation in emotion and cognition among fishes Felicity Huntingford

Variation in emotion and cognition
among fishes
Felicity Huntingford & Victoria Braithwaite
University of Glasgow, Glasgow, U.K.
Penn State University, PA, U.S.A.
Requested topics
• What are the cognitive capacities of fish and do
fish experience emotions?
• Are the answers the same for different kinds of
fish?
• If not, what are the implications for fish welfare?
Issues to address
• Concepts of cognition and
emotion
• Kinds of evidence for
cognitive and emotional
capacity in non-human
animals
• Status of the evidence for
fish
• Variability in cognitive and
emotional capacity among
fish
• Implications for welfare
About definitions
of welfare
• To address public concern fully requires consideration of
not just the functional responses fish make to challenge
but also what they feel
• Nor easy, because ultimately it is impossible to know
what a fish (or any non-human animal) feels
• The best we can do is to gather as many sources of
indirect evidence as possible about their emotions and
cognitive capacities and draw deductions from these.
• Hence this meeting?
Emotion and cognition
Emotion: Psychological processes arising when an
animal experiences something as positive or rewarding
or negative/punishing. Evolved adaptations, enabling
animals to gain rewards or desirable resources and to
avoid danger and harm.
“Adaptive, motivational affective states”
Cognition: The processes by which an animal
internalises information about past experience and
present conditions and adapts subsequent behaviour
accordingly. Involves perception, learning and memory
Many links between emotion & cognition
COGNITIVE PROCESSES
COGNITION
EMOTION
PERCEPTION
LEARNING & MEMORY
Interpretation of information, which depends on past
experience, changes with emotional state, which in
turn alters in response to interpreted information
Evidence for cognitive and emotional capacity in
non-human animals
Central nervous system: homologous brain machinery to that
known to control cognition and emotions in humans?
• Neuroanatomy
• Neurochemistry
Behaviour (and physiology)
• Response to negative or positive stimuli
• Priorities and choices
• Ability to learn
• Complexity and flexibility
• Goal directedness
• Anticipation
Burns: The capacity to “guess and fear”
Brain: behaviour links
Status of fish: neuroanatomy
• The lateral and medial pallial regions
of the teleost forebrain are
homologous to the mammalian
hippocampus and amygdala, which
are involved in learning and
emotions in mammals, even though
they develop in a different way
Broglio et al. 2003, 2005.
• Caution is required about
using such evidence (either
way) based on structure
alone: assumes equivalence
of function over
evolutionary time
Status of fish: neurochemistry
Dopaminergic and serotoninergic systems in fish
Green
= dopaminergic
Dark blue = noradrenergic
Orange = serotoninergic
Panula et al 2010
Behavioural complexity: status of fish
Well developed capacity for learning
No shock
Shock
Trace Pavlovian
conditioning with
reinforcer devaluation
Nordgreen et al. 2009.
Latency to feed (sec)
10
8
6
4
2
0
1
2
Training
3
4
5
Devaluation
Trace avoidance
conditioning
Portavella et al 2002.
Complex, flexible behaviour
indicative of well developed cognitive capacity
• Bystanders and transitive inference
Transitive inference:
A>B B>C C>D D>E so B>D etc
Grosenick et al. 2007
• Reciprocity. Tit-for-tat
• Groupers and eels
Complex, flexible behaviour
• Self-control/impulse control
• Optimal diet choice
• Reverse reward
contingency
What about positive emotions?
• Removal of ectoparasite
• Appetance for aggression
• Nests and goal directedness
Danisman et al 2010
Status of fish: brain-behaviour links
Evidence from lesion experiments that the hippocampusand amygdala-equivalents play a role in learning and
emotions respectively in fish
Spatial accuracy index
Proximal cues removed
0.8
0.7
0.6
0.5
Sham
MPX
LPX
Duran et al 2010
Summary of forebrain function
in fish and mammals
Broglio et al 2005
Striking similarity of function
Evidence for role of dopamine
in reward and learning in fish
Reinforcing effects of SP
(dopamine) administration
SP (dopamine) mediation of
discrimination learning
SP
450
Unpaired
Paired
100
50
0
-50
-100
Control
SP25
SP50
Matioli et al. 1993
SP50
+DAant
Time to find food (sec)
Before-after time (sec)
150
SP+DAant
350
250
150
50
0
Train
Test
Rev1
Rev2
1
2
3
4 Rev3
5 Rev4
6
Matioli et al. 1997
So far:
• Concepts of cognition and emotion
• Evidence for cognitive and emotional capacity
in non-human animals
• Status of the evidence for fish
Fish are not mindless robots responding to challenge by
simple reflexes with no emotional or cognitive content
They are capable of complex behaviour indicative of
complex cognitive abilities
Still to make an explicit link between cognitive and
emotional status and capacity for suffering or pleasure in
fish: work so far necessary but not sufficient
• Variability in cognitive and emotional capacity among fish
• Implications for welfare
Sources of variability in
emotional and cognitive
capacity among fish
Within species
• Gender
• Life history stage
• Life history strategy
• Population/strain
• Individuals
Between species
Variability in emotional and
cognitive capacity potentially
has implications for welfare
Within species: gender
• Gender differences in emotional (and possibly cognitive)
capacities, certainly in adults but even in juveniles
• Dramatic remodelling
of brain biochemistry and
behaviour when fish
change sex
Larson et al 2003
Bioamine activity
4
Medial pallium
NE
DA
3
2
1
0
1
2
3
4
Days from start of sex change
Female
Non territorial
Male
Territorial
Within species: life history stage
100
As fish grow, they move
through predation windows
In piscivorous species,
above a certain size, prey
become predators
Percentage in diet
Zooplankton
80
Insect nymphs
Fish
60
40
20
0
1
2
3
Time
over
year4 1
With associated changes in
risk and response to it
% change from control
100
5
6
small
large
50
0
Large
Small
Large
Small
-50
-100
Moving
Spines raised
Feed latency
Harvey & Brown 2004
Within species: life history strategy
Male
Parr
Anad
Female
Parr
Anad
Relative brain size
-0.2
MA
FMP
FA
-0.3
-0.4
-0.5
Gender and mating strategy
Relative cerebellum size
• Differences in age of
maturity and mating
strategy within cohorts
• Striking differences in
behaviour
• Differences in relative size
of whole brain and
cerebellum in male and
female trout adopting
different mating strategies
MMP
1.7
1.65
1.6
Mature parr
Anadromous
Kolm et al. 2009
Within species:
individual stress coping styles
Adrenaline
Noradrenaline
• Two kinds of wild brown trout
• Differ in risk-taking and aggression
• And in stress physiology
• “Proactive” and “reactive”
Dopamine
Adrenaline
Brelin et al. 2008
Within species: populations
• Different proportions of
proactive and reactive
fish in laboratory-reared
trout from large, stocked
river and small, unstocked
streams.
% proactive fish
50
40
30
20
10
0
Dalaven
Norm/Jorl
4
• Associated with
differences in response
to hypoxia
Escape attempts/min
D
2
1
0
Brelin et al. 2008
NJ
3
100-70
1
2
50 3
4
30
5
206
Oxygen saturation (%)
7
8
Within species: population
differences in learning
Sticklebacks from river and pond populations given the
opportunity to find food using visual landmarks or direction
of water flow
• River fish use flow
• Pond fish use
landmarks
Percentage of fish
100
Landmarks
Flow
80
60
40
20
0
River
Pond
Braithwaite & Girvan 2003
So far:
• Because of indeterminate growth rates and flexible
sex determination (among other things), in fish more
than in other vertebrates there is much variation in
behaviour, physiology and brain function within a
species.
• This is relevant to welfare, generating different
responses to important challenges, with
associated differences in mortality risk .
Between species:
emotion and cognition
Response to predation risk: 3 and 9 spined
sticklebacks. Differences in response to risk
(fear) in many contexts related to relative
predation risk.
Differences in learning: 3 spined
sticklebacks, but not 9 spined
sticklebacks, alter their behaviour in
response to paternal chases
Even among closely related teleosts,
emotional responses and cognitive
capacities are variable, in relation to
ecological factors.
Between species:
overall brain size
Pelagic fish
Sharks
Teleosts
• Striking variability in
overall brain size.
• Largely due to body size
• But not entirely
Linsey & Collin 2006
Difference in relative size
of brain regions
North American shiners
% variability
Between species:
specific brains regions
Kotreschal et al. 1998
And in rates of evolution of
different brain regions
(Tanganyikan cichlids)
Gonzales-Voyer et al 2006
Olfactory bulb
Telencephalon
Partly related to taxonomy
Ray
finned fish
Lobe
finned fish
Partly related to ecology
Trophic status
• In fish generally, prey species have
larger brains that do their
associated predators
• Larger-brained predators tend to
hunt larger-brained prey.
• Complicated relationship between
trophic level and brain size Kondoh
2009.
Brain/body size predator
• Cichlids that feed on sessile food items have larger brains than
those feeding on motile prey. Gonzalez-Voyer et al. 2009
Brain/body size prey
Social organisation
• In Tanganyka cichlids, the
telencephalon tends to be
larger in mongamous than
polygamous species.
• Monogamous species
have greater visual acuity,
but fewer social
interactions.
Pollen et al. 2007
Stumway 2008
Habitat complexity
Habitat complexity is associated with a larger cerebellum
(more complex movement) and telencephalon (additional
computational capacity)
Pollen et al. 2007
Telencephalon
Sand
Cerebellum
Rock
Sand
Rock
Rock dwelling species have a relatively larger
telecephalon and cerebellum, better visual acuity and
better ability to use spatial cues to find food.
Telen
Cereb
Midbr
Hypoth
Time to find (sec)
3200
Rock
Sand
2400
1600
800
Brain
Medulla
Olf bulb
0
1
2
3
Landmark
Shumway 2008a
4
Some conclusions
• Not clear how much of this variability represents inherited
adaptation and how much is the effect of plasticity in brain
growth.
• Level of analysis is still very crude.
• Size is not everything.
• All the same, comparative studies of brain, ecology and
behaviour throw light on the selective forces that shape the
evolution of brain structure and of cognitive ability.
• Evolutionary biologists can (are starting to be able to) predict
from taxonomy, habitat, diet and social organisation how
complex a fish’s brain and behaviour are likely to be.
So what?
Implications of this variability for welfare
Linking welfare to cognition and emotion
Welfare scientists can use variability in emotion, cognition and
underlying brain machinery in fish (both between and within
species) to probe the difficult relationship between
behavioural complexity, brain structure and welfare.
COGNITIVE PROCESSES
COGNITION
EMOTION
PERCEPTION
LEARNING & MEMORY
Implications of this variability for welfare:
Can fish suffer and enjoy?
• The is no “one size fits all” answer to the general
question of whether fish can suffer of feel pleasure. This
will depend in any given case on the general cognitive
and emotional capacity of the species (and life history
stage etc) concerned.
• Nor is there a single answer to the specific question
of what circumstances will cause a given species of
fish suffering or pleasure. This will depend on specific
cognitive and emotional systems of the species (and
life history stage etc) concerned.
Choosing subjects for welfare-friendly exploitation?
• Does what is known about variable emotional and cognitive
capacities in fish help in drawing a line between animals
whose welfare does and does not matter?
Almost certainly not, partly because a clear line probably
does not exist and partly because we do not have
sufficiently precise tools to locate it (yet?). But fish might
be ranked by susceptibility to poor welfare
•
Could we perhaps get to the point of having “look up”
tables for which species, strain or life history stage and
life history strategy to use for any given purpose to
minimise suffering?
Almost certainly not, but thinking about this might help
to identify the important gaps in knowledge