# Learning, Memory & Reversal Learning in Octopus

> Part III: Intelligence in Action · Chapter 3 of 17 — The Octopus Mind
> Canonical: https://octopuscognition.org/sections/learning-memory-reversal-learning-in-octopus/

## In brief

Octopuses learn by nearly every paradigm tested. Foundational mid-20th-century work by J.Z. Young, Brian Boycott, and Martin Wells at the Naples Zoological Station established that Octopus vulgaris readily acquires associative and operant discriminations: presented with an object plus food (reward) or a mild electric shock (punishment), animals learn…

Octopuses learn by nearly every paradigm tested. Foundational mid-20th-century work by **J.Z. Young, Brian Boycott, and Martin Wells** at the Naples Zoological Station established that *Octopus vulgaris* readily acquires **associative and operant discriminations**: presented with an object plus food (reward) or a mild electric shock (punishment), animals learn within tens of trials to attack or retreat. Wells and Young dissected two anatomically separable learning systems (Wells & Young, *J. Exp. Biol.*, 1960s). **Visual discrimination** (shapes, orientation, brightness, size) is handled by the **optic lobes**, encoding stimuli by the *pattern* of receptors excited; **tactile discrimination** (texture, but notably *not* shape or weight, which the arms cannot represent) resides in the **inferior frontal/subfrontal lobe system**, encoding the *proportion* of chemo-tactile receptors excited. The **vertical lobe (VL)** sits atop both systems and functions as a shared memory/consolidation station rather than a primary sensory analyzer.

**Reversal learning** demonstrates genuine cognitive flexibility beyond simple discrimination. Historically, Wells found VL-lesioned animals were impaired specifically at *reversing* an established rough/smooth tactile discrimination. Modern work is methodologically careful: **Bublitz, Dehnhardt & Hanke (2021, *Front. Behav. Neurosci.*)** trained *O. vulgaris* on a left/right spatial reversal task—animals completed **2–13 successive reversals**, with the best performer reaching 13. Critically, octopuses given *positive reinforcement only* often **failed to learn at all**; introducing an explicit **incorrect-choice signal (ICS)** transformed performance, letting them solve the task in a few sessions and progressively reduce errors across reversals (serial reversal improvement). Bublitz et al. (2017, *Front. Physiol.*) earlier cautioned that many older "reversal" claims conflated methodology with cognition—so the flexibility is real but the classic literature is partly contested.

**Spatial learning and navigation** are well documented. **Boal, Dunham, Williams & Hanlon (2000, *J. Comp. Psychol.*)** gave *Octopus bimaculoides* one open escape burrow among six; animals learned the location and **retained it for ~1 week**, and reduced movement over exposure consistent with exploratory/latent learning. **Moriyama & Gunji (1997, *Ethology*)** showed maze/detour solving, with animals shifting from inefficient tactile groping to efficient swimming. Field and lab work by **Jennifer Mather** established that foraging octopuses use route-based spatial memory and even show landmark use during homing.

Memory is **biphasic**. Sanders and Young's lesion studies showed a **short-term** phase and a distinct **long-term** phase. Sanders (1970) quantified long-term tactile retention: performance fell **25% by 8 days, 50% by 24 days, 75% by 53 days, and 90% by 96 days**—true multi-month memory. VL removal spares acquisition and short-term recall but degrades long-term storage, dissociating the two systems.

The **cellular basis of consolidation** is the field's crown jewel, driven by **Binyamin Hochner's** Hebrew University lab. Using a VL slice preparation, **Hochner et al. (2003, *J. Neurophysiol.*)** found a robust, **activity-dependent, vertebrate-hippocampus-like LTP** of glutamatergic field potentials at the superior-frontal-lobe (SFL)→amacrine synapse—striking convergent evolution. **Shomrat, Zarrella, Fiorito & Hochner (2008, *Current Biology*)** linked this LTP causally to behavior via a **passive-avoidance task** (attacking a negatively reinforced red ball; paradigm from Sanders & Barlow, 1971): **tetanizing** the VL tract *accelerated* short-term learning while **transecting** it *slowed* learning, yet **both manipulations impaired next-day long-term recall**—proof the VL and its LTP are required specifically for **consolidation**, not acquisition. Surprisingly for a vertebrate parallel, this LTP is **NMDA-receptor-independent**; the Hochner group (Turchetti-Maia, Stern-Mentch and colleagues, ~2019–2024) identified a novel **nitric-oxide (NO)-dependent "molecular memory switch"**: activity persistently activates NO synthase, producing presynaptic facilitation of glutamate release—NOS inhibitors block long-term LTP expression.

**Connectomics** (**Bidel, Meirovitch, Hochner et al., 2023, *eLife***) mapped the VL's **~25 million neurons**: **89.3% simple amacrine interneurons (SAMs, ~22 million)** plus a newly discovered **~1.6% complex amacrine (CAM)** class. Remarkably, each SAM receives **only a single synaptic input** on a non-bifurcating neurite—a massive **1:12 "fan-out" expansion** unlike the convergent "fan-in" of the cerebellum or insect mushroom body, suggesting an independently evolved associative architecture.

Octopuses also show **observational learning**: **Fiorito & Scotto (1992, *Science*)** reported naïve observers, after watching a trained demonstrator, selected the same colored ball and did so faster than by direct conditioning—an early (if debated) claim of social learning in an invertebrate. Open questions: the reality/mechanism of observational learning, whether octopuses form spatial "cognitive maps" versus route memories, and how a lobe-based memory relates to distributed arm-nervous-system learning.

**Striking / counterintuitive:**
- Octopus vertical-lobe LTP is strikingly hippocampus-like yet NMDA-receptor-INDEPENDENT, instead relying on a nitric-oxide 'molecular memory switch' — convergent function, different molecular hardware.
- In reversal learning, octopuses given only positive reinforcement often fail to learn; adding an explicit 'wrong-choice' signal is what unlocks flexible learning (Bublitz et al. 2021).
- The VL connectome shows a 1:12 'fan-out' where each amacrine interneuron gets just a SINGLE input — the opposite of the convergent 'fan-in' seen in the cerebellum and insect mushroom body, implying independently evolved associative circuitry.
- Blocking OR over-driving (saturating) VL plasticity both wreck next-day memory while having opposite effects on same-day learning speed — a clean dissociation of acquisition from consolidation.
- Octopus arms cannot learn object shape or weight by touch — the tactile system encodes only the proportion of receptors firing, so it discriminates texture but is 'blind' to geometry.
- Tactile memory is genuinely long-term: measurable retention persists for months, decaying only ~50% at 24 days and ~90% at 96 days.

**Open questions:**
- Is Fiorito & Scotto's (1992) observational learning genuine social learning, or explainable by simpler stimulus-enhancement/local-enhancement mechanisms? It remains debated and imperfectly replicated.
- Do octopuses form true allocentric 'cognitive maps' during navigation, or rely on route memories and egocentric/landmark strategies?
- How does centralized vertical-lobe memory integrate with learning distributed in the arm/peripheral nervous system (which contains ~2/3 of neurons)?
- What is the full molecular cascade of the NO-dependent LTP switch and how does it achieve months-long persistence without NMDA receptors?
- What is the functional role of the newly discovered complex amacrine (CAM) cell class in the vertical lobe circuit?
- How comparable are learning capacities and memory mechanisms across octopus species (most mechanistic work is on O. vulgaris) and between octopus, cuttlefish, and squid?

*Key researchers/labs: Binyamin Hochner (Hebrew University of Jerusalem) — vertical lobe electrophysiology, LTP, consolidation, Graziano Fiorito (Stazione Zoologica Anton Dohrn, Naples) — learning paradigms, observational learning, Octopus vulgaris model, Tal Shomrat — VL LTP and behavioral consolidation studies, Martin J. Wells (Cambridge) — classic tactile/visual discrimination and lesion work, J.Z. Young & Brian Boycott (UCL) — foundational octopus brain and memory-system anatomy, Jennifer A. Mather (University of Lethbridge) — foraging, spatial memory, cognition and behavior, Frederike D. Hanke & Alexandra Bublitz (University of Rostock) — modern reversal and spatial learning, Jean G. Boal — cephalopod spatial learning and navigation, Yaron Meirovitch / Flavie Bidel — VL connectomics.*

### Key papers
- **Shomrat T, Zarrella I, Fiorito G, Hochner B (2008).** *The Octopus Vertical Lobe Modulates Short-Term Learning Rate and Uses LTP to Acquire Long-Term Memory.* Current Biology — Causally links vertical-lobe LTP to memory consolidation: tetanizing or transecting the VL tract both impair long-term recall while oppositely affecting short-term learning rate.
- **Hochner B, Brown ER, Langella M, Shomrat T, Fiorito G (2003).** *A Learning and Memory Area in the Octopus Brain Manifests a Vertebrate-Like Long-Term Potentiation.* Journal of Neurophysiology — First demonstration of robust, activity-dependent, hippocampus-like LTP in an invertebrate brain slice — a landmark case of convergent evolution.
- **Bidel F, Meirovitch Y, Schalek RL, ... Hochner B (2023).** *Connectomics of the Octopus vulgaris vertical lobe provides insight into conserved and novel principles of a memory acquisition network.* eLife — Maps ~25 million VL neurons and reveals a unique single-input, 1:12 fan-out feedforward circuit distinct from cerebellum and mushroom body.
- **Boal JG, Dunham AW, Williams KT, Hanlon RT (2000).** *Experimental evidence for spatial learning in octopuses (Octopus bimaculoides).* Journal of Comparative Psychology — Demonstrates that octopuses learn and retain (~1 week) the spatial location of an escape burrow, evidence of true spatial learning.
- **Bublitz A, Dehnhardt G, Hanke FD (2021).** *Reversal of a Spatial Discrimination Task in the Common Octopus (Octopus vulgaris).* Frontiers in Behavioral Neuroscience — Shows serial reversal learning (up to 13 reversals) and that an incorrect-choice signal is critical — flexibility beyond mere discrimination.
- **Fiorito G, Scotto P (1992).** *Observational Learning in Octopus vulgaris.* Science — Controversial early claim that naïve octopuses learn a discrimination by watching trained demonstrators, faster than by direct conditioning.
- **Sanders GD (1970).** *Long-term memory of a tactile discrimination in Octopus vulgaris and the effect of vertical lobe removal.* Brain Research — Quantifies multi-month tactile memory decay and shows vertical-lobe removal selectively degrades long-term retention.
- **Wells MJ, Young JZ (1960s).** *Centres for Tactile and Visual Learning in the Brain of Octopus; A Touch-Learning Centre in Octopus.* Journal of Experimental Biology — Establishes anatomically separate tactile (inferior frontal/subfrontal) and visual (optic lobe) learning systems with the vertical lobe as shared memory store.
- **Bublitz A, Weinhold SR, Strobel S, Dehnhardt G, Hanke FD (2017).** *Reconsideration of Serial Visual Reversal Learning in Octopus from a Methodological Perspective.* Frontiers in Physiology — Critically re-examines classic reversal studies, arguing methodology inflated some cognitive-flexibility claims.
- **Turchetti-Maia AL, Stern-Mentch N, Hochner B, et al. (2024 (bioRxiv)).** *A novel nitric oxide (NO)-dependent molecular switch mediating LTP in the Octopus vulgaris brain.* bioRxiv preprint — Identifies NO/NOS as the presynaptic mechanism of VL LTP, explaining its NMDA-independence.

## Resolved source links

- [The Octopus Vertical Lobe Modulates Short-Term Learning Rate and Uses LTP to Acquire Long-Term Memory.](https://doi.org/10.1016/j.cub.2008.01.056) — DOI 10.1016/j.cub.2008.01.056
- [A Learning and Memory Area in the Octopus Brain Manifests a Vertebrate-Like Long-Term Potentiation.](https://doi.org/10.1152/jn.00645.2003) — DOI 10.1152/jn.00645.2003
- [Connectomics of the Octopus vulgaris vertical lobe provides insight into conserved and novel principles of a memory acquisition network.](https://doi.org/10.7554/elife.84257) — DOI 10.7554/elife.84257
- [Experimental evidence for spatial learning in octopuses (Octopus bimaculoides).](https://doi.org/10.1037/0735-7036.114.3.246) — DOI 10.1037/0735-7036.114.3.246
- [Reversal of a Spatial Discrimination Task in the Common Octopus (Octopus vulgaris).](https://doi.org/10.3389/fnbeh.2021.614523) — DOI 10.3389/fnbeh.2021.614523
- [Observational Learning in Octopus vulgaris.](https://doi.org/10.1126/science.256.5056.545) — DOI 10.1126/science.256.5056.545
- [Long-term memory of a tactile discrimination in Octopus vulgaris and the effect of vertical lobe removal.](https://doi.org/10.1016/0006-8993(70)90154-x) — DOI 10.1016/0006-8993(70)90154-x
- [Centres for Tactile and Visual Learning in the Brain of Octopus; A Touch-Learning Centre in Octopus.](https://doi.org/10.1242/jeb.38.4.811) — DOI 10.1242/jeb.38.4.811
- [Reconsideration of Serial Visual Reversal Learning in Octopus from a Methodological Perspective.](https://doi.org/10.3389/fphys.2017.00054) — DOI 10.3389/fphys.2017.00054
- [A novel nitric oxide (NO)-dependent molecular switch mediating LTP in the Octopus vulgaris brain.](https://search.crossref.org/?q=A%20novel%20nitric%20oxide%20(NO)-dependent%20molecular%20switch%20mediating%20LTP%20in%20the%20Octopus%20vulgaris%20brain.)

## Related trails

- [Intelligence in Action](https://octopuscognition.org/trails/intelligence-in-action/index.md): Which celebrated octopus abilities survive close methodological scrutiny?