Transcript Does learning vary with body temperature in a eurythermic

Does learning vary with body
temperature in a eurythermic lizard?
Researchers:
R. Anderson, W. Boyle, R. Cockrel, O. Munzer, A. Segars
Western Washington University
Subject Species:
Elgaria coerulea,
the northern alligator lizard
Effects of body temperature on learning in Elgaria
coerulea: Habituation of OKR
• Learning is:
– a durable, relatively permanent modification of behavior that occurs
through practice or experience, and is usually adaptive (presumably
improves fitness).
• Habituation is:
– perhaps the simplest form of learning.
– the response decrement resulting from repeated stimulation
– learning not to respond to a specific stimulus that has occurred
frequently without significant consequences (nonassociative learning)
• Habituation is useful because
– the animal no longer wastes attention, time or energy responding to the
stimulus;
– not responding also is less likely to draw the attention of the individual to
other animals (predators or prey).
• Habituation is not the same as a simple loss of responsiveness to a
stimulus from sensory adaptation or fatigue.
Learning in Elgaria coerulea:
Non-Associative Learning:
Habituation of OKR
• One device used to study habituation is one that provides
optokinetic stimulation. It is a cylinder with a series of
vertical black and white stripes along its inner surface.
• The cylinder is placed vertically with the stationary subject
animal in the center-bottom, and the cylinder revolves so the
vertical stripes move around the subject animal,
horizontally, across its visual field.
• Response to this optokinetic stimulation, named the
optokinetic response (OKR), may be universal in all
vertebrates (DuLac et al. 1995) and has been examined in a
diverse array of animals, including teleost fish, turtles, lizards
and humans.
The device that stimulates or “releases” the
Optokinetic Response (OKR)
OKR
Stimulator
Habituation of the OKR
• The most commonly studied OKR is “head” OKR because the
behavior is readily evident.
• Head OKR occurs when the individual follows the stripes with
oscillatory head movements; the head drifts laterally with the
stripe movement, then quickly resets back to a central or
forward position.
• The study of habituation of head OKR is a measure at the
whole organism level.
• The whole organism level is more directly relevant to the
ecology of learning than studying organ systems and/or
cellular mechanisms (Bennett and Huey 1990).
• Studying head OKR should be an effective means of testing
the relationship of learning to body (brain) temperature in
lizards and other poikilotherms.
“Cooperative subject” in the OKRS
Northern Alligator Lizard, Elgaria coerulea
E. coerulea is eurythermic, cool-bodied; relatively slow moving.
Undergraduate co-researchers: Amanda Segars, Olivia Munze
Relative performance values
The performance patterns for learning at ecologically relevant body
temperatures in the lizard, Elgaria coerulea are not readily predictable.
Green = slow rise in performance
ability with temperature to a broad
peak (optimum) coinciding near the
center of the behaviorally regulated
temperature range, then a drop in
performance as body temperature
rises above the regulated range.
Field Active Tb
Blue = rise in performance ability
through and above the preferred
temperature range to about the
upper limit of temperature
observed for field-active animals,
then a sharp drop in performance
when temperatures cause severe
dysfunction.
100%
?
?
29oC
50%
18oC Body Temperature Scale
38oC
The effect of body temperature on optokinetic
response: habituation of the alligator lizard, Elgaria
coerulea.
• Two Experiments, both 6 revs per minute (3.7 stripes/ sec):
– Initial Experiment:
• Body temperatures 22, 26, 30oC
10 consecutive minutes at each temperature
CCW cylinder rotation only
anecdotal fatigue check
Follow-up:
• Body temperatures 19, 24, 29oC
9 consecutive minutes at each temperature:
1st set: 4 min, CCW
2nd set: 4 min, CW (and fatigue check)
3rd set: 1 min, CCW (fatigue check)
The effect of body temperature on optokinetic response:
habituation of the alligator lizard, Elgaria coerulea.
(Values are means of head resets for each 15-second interval )
Head Resets per 15 sec
20
(N= 18, 11, 13 at 22, 26, 30oC).
o
22 C,
o
22 C,
o
26 C,
o
26 C,
o
30 C,
o
30 C,
15
habituating
habituated
habituating
habituated
habituating
habituated
10
5
0
0
100
200
300
Elapsed Time (sec)
400
500
600
Data for intervals of 105-120 and 120-135
seconds are excluded to enable visual
separation of habituating and habituated
phases.
Habituation rates for Elgaria coerulea
in Optokinetic Response, OKR at 3 temperatures.
The more negative the slope, the faster the habituation of head re-sets.
0.00
Symbols are means of slopes, bars are SD,
Ns are 18, 11, and 13, in order of ascending temperature
* indicates significantly difference for time to habituation
Habituation slopes
-0.05
-0.10
-0.15
148min*
124min
-0.20
ANOVA for slopes: F2,42 = 8.7, P = 0.002
114min*
-0.25
22oC
26oC
30oC
Rate of OKR habituation is greater and time to reach habituation
is shorter at the higher body temperature in Elgaria coerulea
2nd Experiment: No fatigue!
20
means for all 3 temperatures:
Head resets per 15 sec interval
18
End ccw = 4, begin cw = 13
End cw = 4, begin ccw = 14
16
14
12
10
Learning at 30oC is 30%
faster than learning at 22oC
8
6
Time to habituation:
o
22 C = 148 + 11 sec
o
26 C = 124 + 9 sec
o
30 C = 114 + 4 sec
4
2
0
20
40
60
80
100
120
140
Time elapsed since onset of OKR response
160
180
Relative performance values
The performance patterns for learning at ecologically relevant body
temperatures in the lizard, Elgaria coerulea are not readily predictable.
Green = slow rise in performance
ability with temperature to a broad
peak (optimum) coinciding near the
center of the behaviorally regulated
temperature range, then a drop in
performance as body temperature
rises above the regulated range.
Field Active Tb
Blue = rise in performance ability
through and above the preferred
temperature range to about the
upper limit of temperature
observed for field-active animals,
then a sharp drop in performance
when temperatures cause severe
dysfunction.
100%
?
?
29oC
50%
18oC Body Temperature Scale
38oC
Effects of body temperature on learning in Elgaria coerulea:
Associative Learning in a Y- Maze
Associative Learning* also known as “trial-error-and-trial-success learning,” and is:
learning to associate a behavior with the consequences of that behavior
(e.g., associating pouncing on a prey item or dipping snout in water, or using a particular refuge with
ingesting prey and allaying hunger or drinking water and allaying thirst, or resting and recovering from exercise)
Associative learning usually requires several to many episodes or trials, in which the animal
eventually cognitively associates (learns) success with one behavior versus failure with another
behavior in the same situation.
There will be a greater frequency of successes as the animal experiences more trials, because
the beneficial behavior is performed more often than the unsuccessful behavior. (success is
reinforcement of benefit, whereas failure is no reward)
Avoidance Learning
is a form of associative learning, wherein the animal learns to not perform a behavior that
has a detrimental consequence or “punishment” in a particular context
(e.g., a chase by a predator or damage from a predator, conspecific, or prey item).
Avoidance learning usually requires only one, two, or a few episodes to acquire the learned
response of reducing or not performing the behavior that leads to the “punishment.”
Avoidance learning can be “active” (avoiding & evading the predator) or passive (aversion to food).
(*in psychology parlance, is similar to “appetitive conditioning,” a variant of “operative conditioning”)
Y-Maze methods challenges
• Five separate attempts by both grad students
and undergrad students over a 10 year period to
study maze learning in lizards in our lab failed to
discern clear patterns in the data.
• There were weak hints of trends related to body
temperature along with overwhelmingly strong
variation in behavior among individual lizards.
• Finally in 2009, R. Anderson & W. Boyle tried a
simplified experiment….
Effects of body temperature on learning in
Elgaria coerulea:
Associative Learning in a Y- Maze
William Boyle,
co-researcher
Refugium
open
blocked
Y-maze Methods, 2009
Two widely separated body temperatures:
21oC
v.
29oC
One trial per lizard at each body temperature
The first trial for half of the lizards was at 21oC
The first trial for half of the lizards was at 29oC
Sample size was 24 individuals:
12 lizards studied in late spring quarter
12 lizards studied in early fall quarter
Y- maze Methods
We varied color of end wall between sides
Half of all lizards were presented with green on right.
Half of all lizards were presented with brown on right.
Both sides had the same dark refugium entrance.
The lizard had to try to enter and begin walking up a
ramp in the box to know whether the entrance was
open or blocked.
More Y-maze methods
On the 1st trial of 5 or 6 trials for that day, the lizard was
permitted a free choice to enter the refugium on either side.
Once a lizard entered a refugium, it was given about 10 minutes
to rest-and-hide before the next trial began.
On the 2nd and later trials the lizard could only enter the side it
chose on the first trial.
The lizard was gently harassed by tapping it at the base of the
tail when it attempted cryptic behavior or if it began moving
away from the Y-end; occasionally taps on the head were
required because it was attempting to climb (always
unsuccessfully, given the smooth walls).
Hence, its reward was resting-and-hiding in the refugium
Y-maze results:
• Strong effects of temperature, trial, and individual lizard on
time taken to enter the refugium (ANOVA).
Lizards at 29oC learned faster than when at 21oC
• At both body temperatures, lizards appeared to realize the refugium
was a “faux refugium” by the 2nd trial (1-trial learning?!):
– They spent significantly longer in the maze before entering the refugium during
the second trial than during the first trial.
– They appeared to be pursuing alternative means of escape, rather than entering
the refugium immediately as they had done in the 1st trial.
– Individuals at putative optimal body temperature, 29oC tried
alternative means of escape more in the 2nd & 3rd trials.
– Individuals at 21oC did not reach peak levels of alternative
means of escape until the 5th & 6th trials.
• For trials 5 and 6, individuals at 29oC entered the refugium
significantly earlier than they did at 21oC. They learned
faster.
Y-Maze Statistics
•
•
•
•
•
Body Temperature:
F = 8.5, P = 0.004
Lizard ID:
F = 3.6, P = 0.0001
Trial:
F = 2.4, P = 0.036
Day order
F = 0.5, P = 0.5
Post hoc test of temperature dependent time difference
= 2.18 , p= 0.004
Mean times to enter refugia (not including long climb episodes):
Trial
1
2
3
4
5*
6*
21C
4.8
9.0
8.3
7.8
9.0
8.2
29C
3.9
6.3
7.4
6.3
5.6
4.2
• At 29oC there were more investigative episodes than at 21oC
at trials 2-3: chi-square = 4.91, P = 0.028
Comparisons? Perspective?
• How do the temperature-related patterns
of learning by Elgaria coerulea compare
with similar temperature-and-performance
patterns of learning in other lizards?
• Answer:
– We do not know, because other careful
studies yet must be performed.…
On-going lab and field studies comparing
among lizards that vary in FAM and
temperature-dependence
• Ongoing:
– Antipredation risk v. vulnerability
– Sprinting Speed
– Bite force & Bite Speed
– Endurance and recovery times
– Agility & Acceleration
– Behavioral responses and learning in a Y-maze
– Rates of habituation via OKR (simple form of learning)
Planned lab and field studies comparing among lizards
that vary in FAM and temperature-dependence
• Planned:
– Reaction Time
– Stalking Behavior, Lunge Distance & Lunging Speed
– T-maze learning (associative learning)
– Exploratory behavior (i.e. curiosity)
– Field study of the microevolutionary consequences of
variation in antipredation risk & vulnerability among
Aspidoscelis tigris.
Gambelia, wislizenii, the Leopard Lizard
Aspidoscelis tigris, the Whiptail
Lizard
Lives in desert scrub
Is a wide, intensive forager
Almost always on the move
Crosses open ground often
Seeks hidden prey under shrubs
Summer
field courses!
Lives in desert scrub
Is an ambush predator
Remains still as it visually seeks prey,
Often stations itself near a shrub
Captures mobile prey as they approach
Lizards as model systems
Lizards that vary in modes of food acquisition (e.g., ambusher,
wide forager) and habitat types should have different sets of
challenges among their four basic tasks.
Identifying and sorting out these phenomena may help us
understand variation among lizards in their capacities for
cognition,
exercise capacity (speed & recovery),
body temperature, and
metabolism,
that is, in the salient features that distinguish birds and mammals
from other vertebrates.