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)

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Many of the same neurotransmitters

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Similar nerve cell types

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Functionally convergent vision (except nautilus)

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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

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Mushroom body

honeybee

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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

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Octopuses

Cuttlefish

Squid

ab tuat o Habituation

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Sensitization

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Classical conditioning

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Instrumental conditioning

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Avoidance learning

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Spatial learning

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Mazes and problem solving

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Perceptual processes in visual learning

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Social learning

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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

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Th Cx iv

iii

orange block!

iii

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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)

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If so, what are the neural substrates and correlates for this faculty?

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Do octopuses use cues from other sensory modalities (e.g., tactile,, chemosensation)) to navigate? g

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Do they integrate such multimodal sensory input during navigation?

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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.

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Distance vision via focusing camera eyes ~ more time to plan for—and act on— far-off salient events/objects within a detailed visual scene.

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Distance vision evolved in tandem with neural circuitryy ffor monitoring g and prediction.

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Distance vision paved the way for the elaboration of new kinds of memory ((i.e.,, episodic p memory). y)

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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).

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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)