07.03.2016
Cognitive abilities of fish
Jonatan Nilsson
Institute of Marine Research
Animal welfare
Animal welfare is an individual’s subjective experience
of its mental and physical state
To judge the experience as positive or negative
requires an ability to be aware its own emotions
1
07.03.2016
Do fish feel pain?
• Pain: ”Pain is an unpleasant sensory and emotional
experience associated with actual or potential tissue
damage, or described in terms of such damage”
• Nociception: “the encoding and processing of
harmful stimuli in the nervous system”
– Nociception is not pain if it is not experienced as
unpleasent
• Requires awareness
Fish fulfill the requirements for nociception
•
Several types of nociceptors (”pain receptors”) in the
skin (touch, heat, chemical,...)
•
Neural networks that connect the nociceptors with the
different parts of the brain.
And
•
Fish has longlasting changes in behaviour after
exposure to assumed painful events
•
Painkillers reduce the effect of (potentially) painful
events.
•
Fish can learn to avoid (potentially) painful stimuli.
Lynne Sneddon 2004 Brain Research Reviews 46 123-130
2
07.03.2016
What are the cognitive abilities of fish?
Do fish have the ability of awareness?
• Rose (and others): consciousness in human is
dependent on neocortex
• Fish do not have neocortex
• Therefore fish lack the neurological prerequisites
for any kind of consciousness
3
07.03.2016
But:
Different brains – homologous brain areas
• Mammals
– Hippocampus (H) important for formation
of conscious memories
– Amygdala (A) important for emotional
memories
• Teleost fishes
– Lateral pallium (LP) homologous with
hippocampus
– Medial pallium (MP) homologous with
amygdala
Fish brain
Human brain
Broglio et al. 2005
Depressed fish?
• High level of serotonin activity in the
mammalian brain is a sign of depression.
Vindas et al., in review
4
07.03.2016
Learning abilities
Habituation
• A very simple form of learning
• An organism decreases or ceases to respond
to a stimulus after repeated presentations
• Animals have inherent fear for some stimuli
– often associated with danger in the wild (e.g.
shadows, sudden movements)
– If they learn that such stimuli are without harmful
consequences, the response decreases
5
07.03.2016
Light regimes during smolt production
To initiate smoltification in salmon, light regime is
changed from continuous to 12:12 dark:light (”winter”)
Parr
24
Hours with light
Smolts
24:0 L:D
24:0 L:D → sea transfer
12
«Winter signal»
12:12 L:D 4-6 weeks
0
Habituation to the ”winter signal” (12:12: L:D, light on)
Increase in O2 consumption
Sudden change in light level frightening for salmon
First time light is switched on after night
Folkedal et al., 2010
6
07.03.2016
Pavlovian conditioning
Time
• Association between 2 stimuli
• One neutral stimulus, e.g. a tone or light, conditioned
stimulus (CS)
– Presented first
• One stimulus that elicits a response without training.
Rewarding or aversive, unconditioned stimulus (US)
• After repeated pairings the CS elicits a response
similar to the US response
Pavlov’s dogs
US
CS
7
07.03.2016
Delay conditioning
-simple
-reflexive
Trace conditioning
-A time gap (trace interval) between the CS and the US
-Dependent on the hippocampus (mammals) / lateral pallium
(teleosts)
-Dependent on an awareness of the CS predicting the US
Human eye blink conditioning (sound-CS, airpuff-US)
Delay conditioning (overlapping CS-US): all subjects conditioned
Trace conditioning (time gap between CS and US): Only people
aware that CS predicted US were conditioned
8
07.03.2016
Learning in cod (Gadus morhua):
long trace interval retention
Nilsson et al., 2008a
Conditioning of
Atlantic cod
Groups of 15 juvenile cod
Light blinks (CS) in the feeding area
predicted delivery of dry food (US)
Unpaired control
Delay conditioning (overlapping CS-US)
Trace conditioning
20, 60 or 120 s between light
blinks and feeding
Light
Feeding
Light
Feeding
Light Trace
Light
Light
Feeding
Trace
Feeding
Trace
Feeding
Nilsson et al., 2008a
9
07.03.2016
Delay conditioned cod
100
75
75
50
50
25
25
% fish in CS/US area
100
% fish in CS/US area
0
100 0
10
20
30
40
50
60
Unpaired
control
0
100 0
75
75
50
50
25
25
10
20
30
40
50
60
Delay
conditioning
0
0
0
10
20
30
Trial
40
50
60
0
10
20
30
Trial
40
50
60
Data from Nilsson et al., 2008a
10
07.03.2016
100
75
75
% fish in CS/US area
100
50
25
During trace interval
% fish in CS/US area
0
100 0
10
20
30
40
50
60
0
100 0
75
50
50
25
25
10
20
30
40
50
60
75
50
50
25
25
10
20
30
40
50
60
60 s
0
100 0
75
0
20 s
25
75
0
100 0
% fish in CS/US area
50
During CS
10
20
30
40
50
60
120 s
0
0
10
20
30
40
50
60
0
10
Trial
20
30
Trial
40
50
60
Data from Nilsson et al., 2008a
Memory retention
□ Before light blinks ● During light blinks
88 days after
delay
conditioning
70 days after
trace
conditioning
Data from Nilsson et al., 2008a
11
07.03.2016
Sign-tracking vs. goal-tracking
Sign-tracking:
The response is
directed at the CS
Goal-tracking:
The response is directed
at the forthcoming US
CS
US
Boakes, 1977
US = water
”Drink” response
US = food
”Eat” response
Sign-tracking: Stimulus substitution
→ Act as if the CS is the US
→ approaches the CS (the sign)
Archer fish:
hunts prey by shooting it down with a jet
of water
Shoots at a CS located above the water
Waxman & McCleave, 1978
From Jenkins & Moore, 1973
12
07.03.2016
Anticipatory behaviour
Goal-tracking
• The predictive signal (CS) brings an explicit
expectation of the forthcoming reward (US), the
response is directed at the location of the reward,
i.e. the goal
• ”Resturant is open”!
10 min break
13
07.03.2016
Sign- and goal-tracking in Atlantic
cod (Gadus morhua)
New, naïve fish!
Light ring
US ring
US
section
CS
section
Automatic
feeder
Nilsson et al., 2008b
14
07.03.2016
CS
CS
US
US
● CS sector
Early trials
○ US sector
Delay
(feeding area)
Late trials
CS
US
CS
US
Early trials
Trace
Late trials
Nilsson et al., 2008b
Delay conditioned halibut
15
07.03.2016
Trace conditioned halibut
Number of fish maintaining their position on the floor during the CS-US
period (filled) and a period of the same duration before the CS (open)
Delay
conditioning
Before the CS
During the
CS-US period
60 s trace
conditioning
Before the CS
During the
CS-US period
16
07.03.2016
Halibut
Delay
Take-offs
Few fish
motionless
Trace
Most fish
motionless
60 s
Repositions
Time from CS onset (s)
Nilsson et al., 2010
Different responses to delay and
trace conditioning
Delay conditioning
• Immediate response
• Do not sign-track
• Swim towards the surface,
i.e. were food will arrive
– Goal-tracking (?)
• Expect food when the CS is
on – fast response
Trace conditioning
• More cautious responses
• Do not sign-track
• Near the floor – not
towards the surface
• Do not expect food when
the CS is on, but some time
after
17
07.03.2016
Cod – a cruising predator
• Cod always approach the signal (CS) immediately
– Delay
– Trace
– Sign-track
• Sign-tracking gives fast responses
• Goal-track some seconds later
Halibut – a ”sit-and-wait” predator
Detection point
Do not swim to the CS
Respond late in trace conditioning
18
07.03.2016
Detection point
Prey moves,
takes some time
Attack point
Detection point
Prey moves,
takes some time
Attack point
19
07.03.2016
Different anticipatory behaviour also
found in
• Rat (search behaviour) and cat (sit-and-wait)
– van den Bos et al., 2003
• Salmon parr (sit-and-wait) and post-smolts
(shoaling, cruising)
– Folkedal, 2010
Trace conditioned rainbow trout
1.
Trace
conditioning
+
Shock
Devaluation
of reward
+
Increased
latency to eat
2.
Control
All controls continued to respond to the
CS-light
3.
Test
4 out of 5 fish with devalued food
stopped responding to the CS-light
→ Fish aware what came after the CS
Nordgreen et al., 2010
20
07.03.2016
From fright to anticipation
Will farmed fish adapt faster to aversive stimuli
if they associate such stimuli with a reward?
+
=
?
Conditioning of salmon
Before
Light flashes
Food
First exposure
Light flash, followed by food
Light flash aversive for salmon
10th exposure
Light flash, followed by food
30th exposure
Light flash, followed by food
100th exposure
Light flash, followed by food
Bratland et al., 2010
21
07.03.2016
Conditioning of cod with a
splashing dip net as the CS
Approach the dip net first and thereafter the feeding area
5 s after ”netting”
25 s after ”netting”
Control
Conditioned
Before
= Netting area
= Feeding area
Nilsson et al., 2012
Operational learning
Learning an association between a
behavioural action and its outcome
22
07.03.2016
Self feeding
Do cod pull because they are rewarded?
Activation rewarded
Activation not rewarded
Learnt after 4 hours
Activation rewarded
Activation not rewarded
Activation not rewarded
(rapid loss of curiosity)
Nilsson & Torgersen, 2010
23
07.03.2016
Evaluation of self-feeders as a tool to study diet
preferences in groups of Atlantic cod (Gadus morhua)
Two self-feeders in each tank, one emptied after 2 weeks
Millot et al., 2012
• Cod swam to feeding area when they saw
other fish activate
• Associate behaviour of other fish with food
Millot et al., 2012
24
07.03.2016
3 individuals started to use the ID-tag as a “tool” to
activate the feeder
Millot et al., 2014
7 final activations
7 first activations
Standadized swimming
pattern
Stopped using the mouth
Days
Come faster to the feeding area
Activations
25
07.03.2016
Tag activations
• Activation with the mouth a natural thing to
do (investigate/eat with the mouth)
• Activations with the tag is not a natural thing
to do
– No natural connection between the back and food
• Demonstrates flexible behaviour
– Invention by operant learning?
Summary
• Do fish have the ability of awareness?
• Responses to potentially painful stimuli
indicate a negative experience (awareness)
– Avoidance, behavioural changes
• Fish can learn tasks that are indicative of
awareness
– Trace conditioning
– Goal-tracking
26