Download The Octopus as a Possible Model for Invertebrate Consciousness

The Octopus as a Possible
Model for Invertebrate
Consciousness Studies
UQÀM
Institut des
Sciences Cognitives
Summer Institute:
Evolution and Function
of Consciousness
Mind, Brain, and David Edelman
Harvard Behavior 92
University
June 28th-July 11th, 2012
Montréal, Canada
The octopus: a tractable test case for the
phyletic
p
y
boundaries of consciousness
•Behavioral flexibility that rivals that of some
higher vertebrates.
•A sophisticated nervous system that in any
case appears lless complex
l iin gross organization
i ti
than that of vertebrates.
•Functionally convergent [NMDA-independent]
[NMDA independent]
LTP and learning and memory faculties that are
comparable to some mammals.
•The diversity of behaviors among octopus
species suggests possible differences in neural
properties driven by selection pressures and/
or environmental context.
1. Consciousness: A working definition
2. Structural and functional properties of
consciousness
3 Invertebrate exceptionalism:
3.
The octopus
4. Investigating consciousness in far-flung
species
5. Distance vision and consciousness:
An evolutionary tale
A unique sensorimotor adaptation…
Video courtesy of Roger Hanlon, MBL
1. Consciousness: A working definition
2. Structural and functional properties of
consciousness
3 Invertebrate exceptionalism:
3.
The octopus
4. Investigating consciousness in far-flung
species
5. Distance vision and consciousness:
An evolutionary tale
Primary consciousness
• The stitching together—or binding—of
many sensory threads into a coherent,
unified ‘world-scene’ and the persistence
of that scene in memory.
memory
• This view allows the possibility of
conscious states in a variety off non-human
h
animals.
• How does this binding actually happen?
A key distinction
 Sensory (primary) consciousness (PC):
 Literally “living
living in the moment
moment”
 The presence of a multimodal scene
 A ‘remembered present’ (G.M. Edelman)
 The ‘specious
specious present
present’ (W.
(W James)
 Higher-order consciousness (HoC):
 A frame of reference seemingly encompassing
past, present, and future
 C
Conscious
i
states that
h reify
if the
h contents off primary
i
consciousness as objects
 A sense of self
 Explicit construction of past and future scenes
1. Consciousness: A working definition
2. Structural and functional properties of
consciousness
3 Invertebrate exceptionalism:
3.
The octopus
4. Investigating consciousness in far-flung
species
5. Distance vision and consciousness:
An evolutionary tale
Some basic criteria for primary consciousness
• Brain regions that function like thalamus and cortex
(i.e., thalamocortical reentrant signaling).
• Dynamic neural activity (firing of neurons across the
cortex)) that
h resembles
bl what
h we observe
b
d
during
i the
h
human conscious state.
• The ability to make sophisticated discriminations,
which would suggest a deep reciprocal connection
between perception and memory.
memory
Edelman (1989) The Remembered Present. Basic Books.
Seth et al.
Consc.. Cogn
Cogn.,
., 14:119
14:119-139;
al (2005).
(2005) Consc
Edelman et al. (2005), 14:16914:169-187;
Edelman and Seth (2009) Trends Neurosci
Neurosci.,
., 32(9):47632(9):476-484.
Properties of consciousness
 Wide range of conscious







contents
Widespread brain effects
Informativeness
R id adaptivity
Rapid
d ti it and
d
fleetingness
Internal consistency
Limited capacity and
seriality
Sensory binding
Self attribution
Reportability
Subjectivity
Focus-fringe structure
Relation to learning
Stability of conscious
contents
 Allocentricity
 Knowledge of the world
and the self
 Coherent neural activity in
th thalamocortical
the
th l
ti l core or
its analog.





Seth et al. (2005). Consc
Consc.. Cogn
Cogn.,
., 14:119
14:119-139
The functional anatomy of consciousness
Edelman et al. (2005). Consc
Consc.. Cogn
Cogn.,
., 14:
14:169
169-187
Higher neural function in invertebrates
(e g consciousness)
(e.g.,
Have similar properties underlying sophisticated
functions and behaviors emerged in nervous
systems—like that of the octopus—which are
radically different from those of vertebrates?
One sensory faculty
faculty—vision—may
vision may offer a clue
clue… and
an opportunity.
Distance vision (acuity at distance)
E (sensory):
Eye
(
)
Liquid-filled, single compartment
Ocular musculature for moving eye
Focusing lens (‘camera-like’)
Photoreceptors within a retinal sheet
()
Neural(?):
Retinal ganglion (vertebrate)
Input fibers (axons)
Thalamic relay (vertebrate; lat. gen.)
Primary visual cortex (vertebrate)
Higher visual areas (vert.; V2, MT,
etc.)
Distance vision (acuity at distance)
E (sensory):
Eye
(
)
Liquid-filled, single compartment
Ocular musculature for moving eye
Focusing lens (‘camera-like’)
Photoreceptors within a retinal sheet
()
Neural(?):
Optic lobe (invertebrate)
Input fibers (axons)
Thalamic relay (vertebrate; lat.
g
genic.)
)
Primary visual cortex (vertebrate)
Higher visual areas (vert.; V2, MT,
Approaches to structure and function
y of nervous systems
y
in a diversity
Scale
Levels of resolution
•The neuron
•Cellular specialization (new
neuronal phenotypes,
supporting cells, i.e., glia,
Schwann cells, etc.)
•Ganglia
•Fused ganglia
•Regional specialization
•Functional circuitry
Levitan & Kaczmarek (2002) The Neuron, Oxford University Press.
The molecular transform of experience
y
in the nervous system
Linden (2007) The Accidental Mind. Harvard University Press.
Caenorhabditis elegans
~20,000 genes
302 neurons
Aplysia Californica
Glanzman Lab, excerpted from NOVA (WGBH)
Adapted from Kandel (1979)
Learning-related
synaptic modification
Invertebrate: presynaptic view
(c. 1995)
Vertebrate: post-synaptic view
NMDA receptor
receptor-dependent
dependent LTP in
Mammalian hippocampus and
cortex
Vertebrate/invertebrate
synthesis: Learning-related
enhancement of glutamatergic
synapses
y p
Adapted from Glanzman (2009) Curr. Biol. 20, R31‐36.
Avoidance conditioning in O. vulgaris
is mediated by
y long-term
g
potentiation
p
Glanzman (2008) Curr. Biol. 18(12):R528.
There are intra- and inter-cellular
mechanisms that are common to
both invertebrates and vertebrates.
1. Consciousness: A working definition
2. Structural and functional properties of
consciousness
3 Invertebrate exceptionalism:
3.
The octopus
4. Investigating consciousness in far-flung
species
5. Distance vision and consciousness:
An evolutionary tale
The octopus
(O. bimaculoides)
Higher vertebrates and cephalopod molluscs
(octopus, squid, cuttlefish, nautilus)
Two very different groups of animals:
• Different developmental pathways
• Different brain organization
•
Different body designs and locomotion
…but with some similarities:
•
Similar genes (FoxP)
•
Many of the same neurotransmitters
•
Similar nerve cell types
•
Functionally convergent vision (except
nautilus)
•
Some comparable learning and memory
faculties
Avian and mammalian brains: structural homology
pallial structures (mammalian cerebral
~ cortex (Cx); avian pallium (Pa))
~ thalamus (Th)
~ hippocampus (Hc)
~ vertical (VL) and median superior
frontal (MSF) lobes
~ striatum (St)
~ midbrain (Mb) and hindbrain (Hb)
~ cerebellum (CB) and peduncle (Pe)
~
retina and retina-like optic lobe
(vertebrate Re; octopus OL)
Cephalopod brains: unfamiliar structures,
analogous functions(?)
The octopus nervous system
Excerpted from ‘Deep Sea Aliens’ (2010) MC4 Productions, Paris, FR
The octopus nervous system
•The nervous system of an average-sized common
octopus (O. vulgaris) contains roughly 500 million
neurons.
neurons
•The CNS of O. vulgaris contains approximately
200 million neurons.
•The central brain of O. vulgaris contains 200 and
10 000 times as many neurons as the brains of Apis
10,000
and Aplysia, respectively.
Flexibility
of behavioural
Sensory and
motor
systems responses
in O. vulgaris
Visual
Tactile
Integrative [?]
After Young (1991); from Borrelli & Fiorito ( 2008)
Courtesy of G. Fiorito, SZN
A suggested difference in functional organization
Zullo et al. (2009) Curr. Biol. 19:1-5.
No [apparent] central topographical organization
underlying motor control of limbs
A suggested difference in functional organization
Zullo et al. (2009) Curr. Biol. 19:1-5.
No [apparent] central topographical organization
underlying motor control of limbs
Animal nervous systems and the problem of embodiment
i.e., What is it like to be an octopus? (apologies to T. Nagel)
Invertebrate analogs
g of
vertebrate neural function
Invertebrate analogs of vertebrate hippocampus?
Hippocampus
?
Mushroom
body
honeybee
?
Vertical
lobe
squid
Divergent anatomies,
anatomies
convergent function:
Learning and memory
Human
Zebra finch
Octopus
HVC
Hc
Pa
HPa
LV
RA
MPa
LMAN
Hc
Cx
LV
NPa
St
X St
APa
Cb
Mb
Pd
Eye
Mb
Th
Eye
Hb
DLM
Re
nxIIts
Hb
Pd
Re
Th
10mm
10mm
Cephalopod molluscs
Birds
Mammals
✔
✔
✔
✔
✔
✔
Octopuses
Cuttlefish
Squid
ab tuat o
Habituation
✔
✗
✔
Sensitization
✔
Classical conditioning
✔
✔
Instrumental conditioning
✔
✔
✔
✔
Avoidance learning
✔
✗
✔
✔
Spatial learning
✔
✗
✔
✔
Mazes and problem solving
✔
✔
✔
Perceptual processes in visual
learning
✔
✔
✔
Social learning
✔
✔
✔
✗
✔
Cb
Observational learning in O. vulgaris:
Still controversial nearly
y 20 years
y
later
After Fiorito and Scotto (1992); clip excerpted from ‘Deep Sea Aliens’ (2010) MC4 Productions, Paris, FR
1. Consciousness: A working definition
2. Structural and functional properties of
consciousness
3 Invertebrate exceptionalism:
3.
The octopus
4. Investigating consciousness in far-flung
species
5. Distance vision and consciousness:
An evolutionary tale
Study of consciousness in distant phyla (i.e., cephalopod
molluscs) ~ Development of correlative lines of evidence
f
from
anatomy, physiology,
h i l
and
db
behavior
h i
(a)
(b)
i
ii
i
ii
?
Th Cx
iv
iii
orange
block!
iii
?
iv
Adapted from Edelman and Seth (2009) Trends Neurosci.
Octopus neurophysiology
Blue LED
Blue LED
Edelman, Gutnick, Kuba, and Zheng (2011) unpublished data
Single-unit recording (spike)
1. Consciousness: A working
g definition
2. Structural and functional properties of
consciousness
3 Invertebrate exceptionalism:
3.
The octopus
4. Investigating consciousness in far-flung
species
5. Distance vision and consciousness:
An evolutionary tale
A [more or less] accepted assumption:
The emergence of eyes was correlated with the
appearance off mobile
descended
bil animals
i l d
d d ffrom
sessile ancestors.
Mobility meant exploitation of far-flung food
sources and, eventually, predatory strategies.
This led to an “arms race” between predator and
prey species in terms of innovations like faster
(and more efficient) locomotion, armor, peptide
mimicry of neuromodulatory signals, and other
defenses, as well as refinements in vision.
Eyes evolved many times; but visual acuity at
distance may be unusual…and very important
Male jumping spider
(Habronattus americanus)
Mantis shrimp
(Odontodactylus scyllarus)
Adapted from Land and Nilsson (2006)
From Fernald (2006) p.1915
From Treisman (2004) p.3825
Octopus vision
• Familiar structure and
function
• Suggestive of [certain]
requisite memory and
integration substrates
• A sensory portal to
exploit for investigating
higher neural function
[Some] evolutionary convergence:
y of coleoid cephalopods
p
p
and vertebrates
eyes
Mammalian retina
photoreceptors
Octopus retina
photoreceptors
Light
Li ht
Light
From Land and Nilsson (2002) Animal Eyes,
Oxford University Press, p. 64.
Wassle and Boycott
(1991)
Ramon y Cajal
Young (1962)
Optic lobe of O. vulgaris
Retina-like
processing(?)
Young (1971)
Plexiform zone
Plexiform zone
Plexiform zone
Choe, McKinstry, Edelman, Grimaldi & Fiorito (2010)
Spatial acuity in vertebrates
and invertebrates
*
*
D.P. Harland and R.R. Jackson (2000) Cimbebasia 16:231-240
Invertebrate psychophysics:
the fruit fly,
fly the bee
bee, and
and…the
the octopus.
from Van Swinderen (2005) Bioessays,
A psychophysical approach allows us to:
•Manipulate temporal and spatial
p
p
p
)
properties
of stimuli ((and p
perception)
•Monitor behavior for changes that
indicate perceptual and integrative
functions at work (e.g., ‘frame rate’
and biological motion studies)
•Identify neural correlates of
perception and integration
•Investigate and monitor possible
conscious states
Salient stimuli for an octopus
Positive
Natural
Artificial
Negative
Motor output ~ Behavioral report
Body patterning
E. Canali, courtesy of Fiorito laboratory
Body posture/movement
D. Edelman, courtesy of Fiorito laboratory
Video presentation of stimuli
D.B. Edelman, courtesy of Fiorito laboratory, Stazione Zoologica Anton Dohrn, Naples, IT
Seq. 1: 60Hz
D.B. Edelman, courtesy of Fiorito laboratory, Stazione Zoologica Anton Dohrn, Naples, IT
Seq. 1: 40Hz
D.B. Edelman, courtesy of Fiorito laboratory, Stazione Zoologica Anton Dohrn, Naples, IT
Seq. 1: 24Hz
D.B. Edelman, courtesy of Fiorito laboratory, Stazione Zoologica Anton Dohrn, Naples, IT
Seq. 1: 12Hz
D.B. Edelman, courtesy of Fiorito laboratory, Stazione Zoologica Anton Dohrn, Naples, IT
Seq. 1: 4Hz
?
D.B. Edelman, courtesy of Fiorito laboratory, Stazione Zoologica Anton Dohrn, Naples, IT
Seq. 1: 0.5Hz
Perception of biological motion
in Octopus vulgaris
A CGI stimulus toolkit: Biological motion
Moving
crab
‘gestalt’
Random
orbiting
dots
(control)
Perception of biological motion in O. vulgaris
Terrestrial visual navigation in the octopus
Maze
template
M
t
l t for
f ttracking
ki
Tracking data
Visual navigation in the octopus
•
Do octopuses have ‘cognitive maps’ (and underlying spatial and
episodic memory functions) comparable to those of mammals?
(see Mather J.(1991)
J (1991) JJ. Comp
Comp. Phys.
Phys A ,168(4):491-497)
168(4):491 497)
•
If so, what are the neural substrates and correlates for this
faculty?
•
Do octopuses use cues from other sensory modalities (e.g.,
tactile,, chemosensation)) to navigate?
g
•
Do they integrate such multimodal sensory input during
navigation?
•
The binding of multimodal input into a unitary ‘scene’ that
persists in memory—as might occur in spatial navigation—would
suggest
gg t a fform off primary
i
consciousness.
i
Distance vision and consciousness:
the rudiments of an argument
•
Animals with focusing [lens], single-compartment, camera eyes ~ more
complex and plastic behaviors than other members of their phyla.
•
Distance vision via focusing camera eyes ~ more time to plan for—and act
on— far-off salient events/objects within a detailed visual scene.
•
Distance vision evolved in tandem with neural circuitryy ffor monitoring
g and
prediction.
•
Distance vision paved the way for the elaboration of new kinds of memory
((i.e.,, episodic
p
memory).
y)
•
Distance vision also allowed the generation of more detailed visual scenes,
which could be broken down into constituent submodal properties (e.g.,
textures,, contours,, intensities,, colors).
) These p
properties
p
would have
necesarily entailed the development of specialized neural architectures and
a higher-order means of integrating them (i.e., higher-order dynamic maps).
•
g
off a unitaryy visual scene,, in combination with new kinds
Integration
of memory and the emergence of a reentrant circuit connecting
perception and [visual] memory (i.e., a thalamocortical loop analog), could
have yielded incipient sensory consciousness.
I gratefully acknowledge the contributions and support of:
The Neurosciences Institute
Donald Hutson
© D.B. Edelman
Thomas Moller
Stazione Zoologica
g
Anton Dohrn
Dr. Graziano Fiorito Piero Amodio
Dr. Luciana Borelli
Michaela Florini
Dr Maria Sirakov
Dr.
Giovanna Ponte
Anna Maria Grimaldi
Ester Canali
Eleonora Sirabella
• What is he doing, and why?
• What
Wh t does
d
h
he see??
• What does he remember?
The common octopus (O. vulgaris)