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. 2023 Jun 16;63(6):1277–1284. doi: 10.1093/icb/icad069

Toward an Understanding of Octopus Arm Motor Control

Cassady S Olson 1,✉, Clifton W Ragsdale 2
PMCID: PMC10755184  PMID: 37327080

Synopsis

Octopuses have the extraordinary ability to control eight prehensile arms with hundreds of suckers. With these highly flexible limbs, they engage in a wide variety of tasks, including hunting, grooming, and exploring their environment. The neural circuitry generating these movements engages every division of the octopus nervous system, from the nerve cords of the arms to the supraesophegeal brain. In this review, the current knowledge on the neural control of octopus arm movements is discussed, highlighting open questions and areas for further study.

Introduction

The motor system enables animals to interact with their environment. How the motor system does this is constrained. The system must reflect the properties of the moving parts, which are composed of biological materials. There should be coordination among muscle groups and, in the case of multiple limbs, across limbs. The incorporation of sensory information, including feedback, is necessary for goal-directed actions and behavioral success. The motor system should be well-suited to its environment to improve the chances of survival and reproduction. Finally, the ability to learn new skills and adapt is critical. The nervous system has provided solutions for the motor control problem in many creatures for very different behavioral tasks, body plans, and environmental contexts. Current research in the motor field is dominated by vertebrate model systems. In taking a comparative perspective to motor control, however, we would likely find emergent properties or even striking differences that provide deep insight to neural motor control beyond what can be gained through vertebrate models alone. We cannot, for example, now say whether having a skeletal system with defined joints, such as those found in arthropods and vertebrates, makes the motor control problem more or less complex. Thus, it is informative to examine how the motor system must change if there is no rigid skeletal support.

Octopuses are fascinating creatures with the ability to control and coordinate eight extremely flexible arms, each with hundreds of suckers. They have an incredibly rich behavioral repertoire (Hanlon and Messenger 2018). They can perform the essential task of prey capture, which involves reaching and grasping with a single arm, or the coordinate action of multiple arms, or an all-eight-arm pounce (Gutfreund et al. 1996; Bidel et al. 2022). Each of these methods also engages the suckers, which can, in turn, move independently. Octopuses can walk, swim, and hunt in rough terrains. They can build shelters and groom themselves. They can even learn novel tasks, such as unscrewing a jar to obtain a crab. This behavioral repertoire provides a fruitful landscape for the study of motor control. How are they able to walk with flexible arms? How are they able to coordinate all eight arms? How are they able to command a single arm to move in isolation? How are they able to control each sucker? How are they able to learn to use their arms in new tasks?

The octopus relies on its central nervous system to drive this extensive behavioral output. There is a large brain located between the eyes, comprising two optic lobes and a central brain, along with an axial nerve cord (ANC), equivalent to a spinal cord, running down the center of each arm. This nervous system is massive. In Octopus vulgaris, the central brain, which wraps around the esophagus, contains 40 million neurons, and the flanking optic lobes contain 130 million neurons, nearly twice as many reported in the mouse brain (Young 1963, 1971; Herculano-Houzel et al. 2006). In addition, the ANCs collectively contain 350 million neurons (Young 1963, 1971). Accordingly, we will consider the current state of octopus arm motor control at the level of arm muscles, arm nervous system, and the central brain. Particular emphasis will be given to open questions and challenges as this is, in large part, a review of what we don't yet know.

Arm muscles

In its most basic form, the motor system controls muscle fiber length-tension relationships. For octopus arm motor control, we must account for what the nervous system is trying to control, that is, the arm itself. Indeed, to understand any final control signals, we need to consider the properties of the muscles. Especially with a limb that can be moved in near infinite degrees of freedom (Kennedy et al. 2020), natural modes of movement could arise from the overall structure of the arm and the biophysical properties of the muscles. Some of these constraints may simplify the control problem.

Each arm is a muscular hydrostat, composed of only muscles, connective tissue, skin, and internal neural tissue. There is no rigid skeleton. The muscles, therefore, both provide structural support and mediate arm movements (Kier and Stella 2007; Kier 2016). Arm movement arises from the brachial musculature, which surrounds the ANC and comprises four muscle groups. In the transverse plane, which is perpendicular to the long axis of the arm, one can readily distinguish these groups (Fig. 1A). The longitudinal muscles run the length of the arm and are thought to be involved in shortening the arm (Graziadei 1971; Kier and Stella 2007; Kier 2016). The transverse muscles are oriented perpendicular to the longitudinal muscles and extend anchoring trabeculae to the edges of the arm. Transverse muscle contraction could elongate the arm. A selective combination of longitudinal muscle and transverse muscle activation is thought to cause bending (Graziadei 1971; Kier and Stella 2007; Kier 2016). There are three bilateral sets of oblique muscles: the outer, middle, and inner obliques. These muscles form sheets tilting away from the longitudinal axis. The handedness of the outer oblique is the same as the inner oblique, but opposite that of the middle oblique. With this arrangement, the obliques are likely to mediate torsion of the arm, though they may also help elongate and shorten the arm (Graziadei 1971; Kier and Stella 2007; Kier 2016). The last muscle group of the arm is the circular musculature. This thin sheet surrounds the other muscle groups and is challenging to discern in transverse section. By their location on the outside of the arm, the circular muscles could constrain movement and may have a role in posture (Kier and Stella 2007; Kier 2012). Connective tissue also plays a fundamental role in supporting the arm (Kier 2012; Clemente et al. 2021); at the least, in the absence of a rigid skeleton, it provides insertion sites for the muscle. Studies indicate that connective tissue wraps around the outside of the arm musculature and surrounds the ANC in the center of the arm (Kier & Stella 2007).

Fig. 1.

Fig. 1

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Muscles of the arm. (A) Brachial musculature. LM (green), longitudinal muscles. TM (yellow), transverse muscles. TR, trabeculae. OMO (purple), outer oblique muscle. OMM (red), middle oblique muscle. OMI (pink), inner oblique muscle. CM (blue), circular muscles. (B) The sucker and its musculature. ACBM (orange), acetabulo-brachial muscles. AC (cyan), acetabulum. INF (magenta), infundibulum.

Sucker movement arises from both the intrinsic sucker musculature and the acetabulo-brachial muscles (Fig. 1B). The sucker musculature, forming the acetabulum and the infundibulum is responsible for the suction and grasping movements of a single sucker. The acetabulum and infundibulum are composed of a three-dimensional array of muscle fibers (Kier and Smith 2002). Suction is achieved by thinning the wall of the acetabulum, a consequence of contracting the radial muscles. Engagement of muscles that act in opposition to radial muscles releases suction (meridional and circumferential muscles; Kier and Smith 2002). The acetabulo-brachial muscles enable sucker stalk movements. These muscles originate from the connective tissue surrounding the arm and insert into the acetabulum. Using the acetabulo-brachial muscles, the sucker, like the arm itself, can orient in the full range of different directions (Kier and Smith 2002).

The biophysical and molecular properties of cephalopod muscles are understudied. Initial investigations demonstrated that the cells are electrically compact—meaning local input influences the voltage potential of the whole cell—and that their inputs are cholinergic (Matzner et al. 2000; Nesher et al. 2019). Investigations into passive and active contractile properties reveal differences between longitudinal and transverse muscles (Clemente et al. 2021; Zullo et al. 2022). Longitudinal muscles appear to have fast activation properties and may be suited to quick movements. Transverse muscles, on the other hand, exhibit slow activation and thus could help maintain posture (Zullo et al. 2022). Further work is needed to investigate these properties in the other muscle groups. Invertebrate muscles possess unique features when compared with vertebrate muscles. In squid, tentacles display a rapid elongation for prey capture, whereas the arms do not. This difference is not due to differences in myosin isoforms, which are usually associated with differences in contractile properties, but rather in the ultrastructure of the muscle (Shaffer and Kier 2016). The transverse muscles in squid tentacles are cross-striated, which allows for rapid elongation, while the transverse muscle mass in squid arm tissue is obliquely striated (Kier 1985). Octopus transverse muscles are also obliquely striated (Shaffer and Kier 2016). This indicates that the contractile properties of the transverse muscles may be akin to those of squid arms and therefore could not produce rapid elongation as seen with squid tentacles. Other unique features of invertebrate muscles include a catch mechanism, which enables prolonged muscle contraction without sustained neural activity. This mechanism is found in cuttlefish papillae and bivalve adductor muscles and is mediated by the protein twitchin (Shelud'ko et al. 2004; Gonzalez-Bellido et al. 2018). We do not know if octopus arm muscles have such a catch mechanism, and study of the molecular composition of octopus muscles may divulge many unique properties.

There exists limited experimental evidence for the coordinated activity of muscles, and current theories leave unresolved questions. For example, even though it is hypothesized that the transverse muscles are involved in elongating the arm, the obliques could also mediate elongation (Graziadei 1971; Kier and Stella 2007). More generally, do these muscle groups work independently or in concert? In squid arms and tentacles and in elephant trunks, there are two sets of obliques with opposite handedness, whereas octopus arms have three (Kier and Smith 1985). In each of these cases, it is thought that the obliques facilitate torsion, but why do octopuses have three, with two of the same handedness? Current hypotheses of arm muscle function only describe movement at a single location, with a bend, twist, or elongation of the arm able to occur at any point along the arm (Kennedy et al. 2020). By contrast, descriptions of activity down the length of the arms in current research are limited to a single arm reach and retraction. During reach, a wave of muscle activity propagates down the arm (Gutfreund et al. 1998), and during retraction, localized collisions of muscle activity create joint-like bends in the arm (Sumbre et al. 2006). While these descriptions capture single arm behavior, they do not provide a basis for generating hypotheses regarding how more complex movements arise. A theoretical framework that could be helpful is that of a long, highly elastic rod. This framework is used in models of octopus arms for application to soft robotics and, more interestingly, perturbations of these models have resulted in movements similar to those of an octopus arm (Chang et al. 2023).

The control system

The extensive octopus nervous system harbors most of its neurons in the arms (Young 1963, 1971). As a result, the nervous system is described as more distributed than that of vertebrates. There is, however, a clear hierarchical arrangement of the control system. For arm movements, lower motor control centers originate in the arm itself. Intermediate motor centers are found in the suboesophageal brain, and higher motor centers reside in the supraesophageal brain (Boycott 1961; Young 1971). We will explore each level in turn.

Arm nervous system

Much of the control circuitry of the arm appears to be in the arm. Amputated arms will move on their own, grasp and reject food, and stimulation of an amputated arm can give rise to behaviors seen in intact animals, such as a full arm reach or movement of a single sucker (Rowell 1963; Sumbre et al. 2001). The arrangement of the arm nervous system has not been rigorously studied since the 1960s. From these studies, it is known that the ANC can be divided into two anatomically distinct territories (Altman 1968; Graziadei 1971; see Fig. 2B). On the aboral side (the side opposite the suckers) sits the cerebrobrachial tract that interconnects the arms and the brain. On the oral side (the side of the suckers) exists a mass of neurons and their processes arranged with the cell bodies on the outside and neuropil on the inside, which is characteristic of invertebrate medullary nerve cords (Richter et al. 2010). At the level of gross morphology, the ANC orients in turn to each sucker, and since most octopus suckers are arranged in two offset rows, the ANC snakes from side to side along the length of the arm (Graziadei 1971). Beyond the ANC, five peripheral nerve centers sit in the arm (Fig. 2A). Situated in the acetabulo-brachial musculature is a sucker ganglion for every sucker. Whether this ganglion is a motor center, sensory center, or both is contested (Rowell 1963; Graziadei 1971; Olson et al. 2021). Located in the four corners of the arm, between the outer and middle obliques, are four intramuscular nerve cords. These intramuscular nerve cords have been described to contain both sensory and motor information for the brachial musculature and may mediate local reflexes (Graziadei 1965, 1971).

Fig. 2.

Fig. 2

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Arm nervous system. (A) Central and peripheral components. ANC (pink), axial nerve cord. IMNC (orange), intramuscular nerve cord. SG (cyan), sucker ganglion. (B) The ANC. Where efferent nerve fibers (blue) travel and where afferent nerve fibers (green) originate, and how both are processed by the ANC, is not known (indicated by question marks). CBT, cerebrobrachial tract. NP, neuropil. CBL, cell body layer. (C) Vertebrate spinal cord. Example of the stretch reflex circuit. Afferent fibers (green) carrying stretch information enter the spinal cord from the dorsal side, excite motor neurons (blue) contracting the agonist muscle, and inhibit (red) motor neurons to the antagonist muscle.

Nerve fibers regularly exit the ANC to connect with the skin, suckers, brachial musculature, and the peripheral nerve centers (Fig. 2B; Altman 1968; Graziadei 1971; Gutfreund et al. 2006). The oral roots, which are reported to carry both sensory and motor information, connect to the sucker ganglion and sucker musculature. While the aboral roots are also reported to carry both sensory and motor information, how these nerves connect to the intramuscular nerve cords and brachial muscles is unknown (Rowell 1963; Gutfreund et al. 2006). The location of motor neurons and how they pool into these nerves is also not known. While claims that each muscle group is innervated separately have been offered, limited experimental evidence supports this proposal (Altman 1968; Graziadei 1971; Nesher et al. 2019). Simply put, we do not know what the full set of neuromuscular units of the arm is.

An important feature of motor control is sensory feedback. Where and how proprioceptive feedback originates in the arm is unclear, and the extent to which octopuses rely on proprioceptive information for arm movements is debated (Gutnick et al. 2011, 2020; Bidel et al. 2022). Despite this, Graziadei (1965) reported the existence of muscle receptors located between the outer and middle oblique muscles, with indications that these receptors feed into the intramuscular nerve cords. He also describes similar cells embedded in the acetabulo-brachial musculature with projections towards the sucker ganglion. The existence of these cells, and their candidate proprioceptive nature, needs further study. Another source of sensory information are the suckers. Sensory receptors receiving chemo-tactile information line the epithelium of the sucker (Graziadei 1962). This information is useful for determining if an object is food. Recent studies have uncovered the existence of chemoreceptors composed of atypical acetylcholine receptors (Albertin et al. 2015; van Giesen et al. 2020). Additional study of the chemo-tactile properties of the octopus sucker apparatus could reveal other novelties in sensory transduction.

The ANC exhibits many similarities to a vertebrate spinal cord (Fig. 2B and C). In a broad sense, they have similar anatomical features: cell bodies, complex neuropil, fiber tracts relaying connections to and from the brain, and regularly exiting nerve fibers. There are also functional similarities. Like an amputated arm freely moving, animals can walk without input from the brain, relying solely on spinal cord circuits (Kriellaars et al. 1994; Whelan 2003; Rossignol and Frigon 2011). This comparison provides a framework to ask questions about the ANC: is there, as in the spinal cord, a loose somatotopic arrangement? Current experiments have shown that the nerve fibers are mixed (Gutfreund et al. 2006), so how is sensory and motor information parsed and integrated? Is there a functional equivalent of the stretch reflex? How are the muscles recruited? Are motor units enlisted incrementally from small to large, as proposed in Henneman's size principle? More broadly, study of how the ANC executes muscle activation and transforms sensory information can inform theories of how the spinal cord might work. Studying the octopus is advantageous as the ANC serves as an easily accessible spinal cord. In a single slice of arm, it is possible to capture the ANC, the full muscle structure, and the sensory afferents.This difference is because the muscles in the arm decrease in size down the length of the arm, but their overall structure remain the same (Kier and Stella 2007). Such a muscle organization implies a pattern of innervation by the ANC akin to the repeated innervation seen in the body segments of a Drosophila larva or annelid worm (Clark et al. 2018). However, no current evidence of a segmental arrangement of muscles in the adult octopus arm exists. Research on the development of the arm musculature could reveal a segmental patterning of muscles that blurs by adulthood, thereby offering insight into patterns of innervation.

Intermediate and higher motor centers

While the arm houses a large portion of the neural real estate, the arm nervous system does not control movement in isolation (Fig. 3). The octopus possesses a large, complex brain with more than three dozen lobes and lobules (Young 1971). The role that the brain plays in motor control has been investigated with Golgi anatomy, electrical stimulations, and lesion studies dating back to the middle of the last century (Wells 1978). As the ANC ascends to the brain, it first branches into the interbrachial commissure. The interbrachial commissure is composed of two bundles of nerve fibers. The first connects each arm to its nearest neighbors, and the second forms a ring, which connects the rest of the arms to each other (Graziadei 1971). Recent evidence indicates that the oral intramuscular nerve cords also connect between arms (Kuuspalu et al. 2022). The kind of information which passes along the commissure and through the connecting intramuscular nerve cords is not known, though it has been suggested that it could be proprioceptive in nature (Kuuspalu et al. 2022). Beyond the interbrachial commissure, the ANC loses its cell body layer as it approaches the brain and coalesces into a nerve known as the brachial nerve. The brachial nerve enters the brachial lobe located in the anterior suboesophageal brain (Young 1971). Along with the pedal lobe, the brachial lobe is considered an intermediate motor center for the control of the arms. It is thought that the brachial lobe exhibits afferent and efferent connections with the arm (Young 1971). Stimulation of the brachial lobe can elicit contraction of multiple arms at once, and stimulation particularly near the site of brachial nerve entry can produce contraction of individual arms (Boycott 1961; Young 1971). Cells from the anterior pedal lobe send fibers to the brachial lobe and into the brachial nerves, and most of the connections appear to be efferent. The main sources of input to the anterior pedal lobe are from the basal lobes of the supraesophogeal brain and the lateral pedal lobe. The lateral pedal lobe in turn accepts afferents from the brachial lobe as well as the basal lobes and the statocysts, which detect vestibular information (Young 1971). While stimulation of the pedal lobe elicits movements of the arms, the lobe also subserves additional motor roles, such as controlling head, funnel and eye movements (Boycott 1961). Further work is needed to sort out the roles of these intermediate motor centers in movement of the arms.

Fig. 3.

Fig. 3

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Simplified account of motor control pathways in the brain and arms of the octopus, emphasizing major connections, and motor hierarchies. Modern evidence for some of these connections, for example, those between the pedal and brachial lobes is not strong. ANC, axial nerve cord.

The higher motor centers are the basal lobes in the supraesophegeal brain. At this point in the motor hierarchy, stimulation will produce coordinated behaviors. In particular, electrical stimulation of the anterior basal lobe of an octopus produces effective walking movements of the arms, as well as eye and head movements (Young 1971). If the frontal supraesophogeal brain is removed with the basal lobes still intact, animals can still walk. However, removing the basal lobes will induce the animal to lie in a heap before finally crawling with sucker movements (Wells 1959; Altman 1968). Stimulation of other regions of the basal lobes will also produce changes in chromatophores, skin papillae, and respiration (Boycott 1961; Young 1971; Zullo et al. 2009).

The pedal lobes possess both contralateral and ipsilateral connectivity with the higher motor centers (Young 1971). No other decussations have been reported deeper in the motor pathway, apart from the interbrachial commissure described above. Interestingly, split brained octopuses demonstrated no obvious impairments in behaviors (Muntz 1961).

Feedforward visual input is vital for orchestrating complex, goal-directed movements. For the octopus, this information has been shown to influence arm choice: when reaching for an object, octopuses most often use the arm that falls in the line of sight between the eye and the object of interest (Byrne et al. 2006). Visual information passes through the optic lobe and then to the peduncle lobe. The anterior basal lobe receives input from both of these lobes, indicating the potential existence of at least two visuomotor pathways (Messenger 1971). Stimulation of the peduncle lobe can elicit locomotor movements of walking and swimming, and lesions of the peduncle lobe have effects on coordinated locomotive abilities (Messenger 1967, 1971). Specifically, while a lesioned animal may be able to recognize prey, its locomotor control is compromised, and profound deficits in posture arise (Messenger 1967). However, animals deprived of vision can navigate normally, indicating that visual input is not essential for movement, whereas peduncle input is (Messenger 1967). These findings indicate that one system is critical for maintaining posture, whereas the other is used for visually guided behaviors. Thus, in many ways, the octopus brain contains a parcellation of motor system function not so foreign from that known in vertebrate systems.

The arms receive a plethora of sensory information, and it is expected that by the time that information reaches the brain, it is highly processed (Rowell 1966). The inferior frontal system (IFS) of the supraesophegeal brain takes in sensory information from the suckers (Young 1971). Only with an intact IFS can octopuses appropriately distinguish between a food and nonfood object, and lesions to the IFS interfere with an octopus's ability to discriminate by touch (Altman 1971). Additionally, lesions to the IFS render the octopus unable to reject objects, as the suckers become sticky (Wells 1961). This indicates that the IFS provides some motor control over suckers, possibly of an inhibitory nature. It is not known how or where proprioceptive information is represented in the brain. Current views dictate that this information does not reach the brain (Rowell 1966). However, given that an octopus can produce coordinated movements in the absence of visual information, proprioceptive input likely reaches the brain in some form.

Clearly, a modern neuroscience cellular and molecular approach to octopus brain motor control is needed. Nevertheless, a few features are already clear. There is an apparent lack of the somatotopy in higher motor centers that is present in vertebrates (Zullo et al. 2009): stimulation of the higher motor centers creates coordinated movement across all limbs, not merely one. This could be due to the nature of the motor control problem in the octopus. Given that arm musculature exhibits a repeated pattern, the same higher order control signal could be used to produce the same muscle contraction regardless of arm. What would then be needed is to relay the signal to specific arms. The brachial nerves issuing from the brachial lobe provide an anatomical pathway to do so. One potential confound is that the diameter of the arm decreases down the length, so the amount of force needed to cause a deflection is monotonically reduced. This problem could be addressed at the level of the ANC. Interestingly, it does appear that sucker sensory-motor control is processed in part by the IFS, and further study is needed to parse this difference. While an absence of somatotopy seems like a departure from vertebrate systems, a similar feature has been shown to be present in vertebrates. Through elevated current stimulation of motor cortex in macaques, Graziano et al. (2002) elicited extensive body behaviors and not just single muscle twitches. A recent fMRI study in primates further suggests a whole body action system embedded within M1(Gordon et al. 2023). As studies of motor control typically center on limited behavioral paradigms, it is possible that a somatotopic map provides a limited view of the functioning of vertebrate motor cortex. Further studies of animals in freely behaving scenarios and of the octopus motor system could provide further insights into alternative computational architectures.

There is a lack of functional recording experiments in the octopus brain. This is partially due to the technical challenges associated with doing such recordings: octopuses are marine creatures that lack hard structures to anchor recording equipment to. Recent technological advances, however, have permitted recordings from the brains of freely behaving octopuses (Gutnick et al. 2023). An additional limitation is the poverty of clear, tractable descriptions of octopus arm behavior. Unlike a vertebrate system, kinematics of octopus arm movement cannot readily be parameterized into features such as joint angles and direction of motion. An alternative approach might be dynamical systems analyses, where internal neural states and how they change are examined at the population level and so should implicitly capture movement parameters (Shenoy et al. 2013). Differences in population states across areas would then likely reflect differences in computational strategies (Russo et al. 2020). Importantly, because this approach is agnostic to specific movement parameters, comparisons between octopus motor center activities and those of other species could be made, leading to new potential insights into motor hierarchies. Ultimately, though, for the octopus, any true understanding of the relationship between the neural control system and the behavior will require a much fuller account of what those motor acts are.

Acknowledgement

We thank Dr. Cindy Chestek and Ms. Amelia Cheng for their comments and National Institutes of Health UF1NS115817 for support.

Contributor Information

Cassady S Olson, Committee on Computational Neuroscience, University of Chicago, Chicago 60637, USA.

Clifton W Ragsdale, Department of Neurobiology, University of Chicago, Chicago 60637, USA.

Conflict of interest

All authors declare report no conflicts of interest.

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