Moving and sensing without input and output: early nervous systems and the origins of the animal sensorimotor organization

The SBT builds on Carl Pantin’s proposal that the earliest nervous systems evolved to coordinate what he called the animal ‘behavior machine’ (1952, 1956). With this phrase he referred to the way in which animals relied on muscle and other contractile tissues such as myoepithelia to generate motility. The SBT explicitly takes contraction-based motility as the kernel of nervous system organization and of the ASMO. This may not seem obvious as many animals have other means of motility, most notably the use of cilia: cellular extensions that can act like small ‘oars’ propelling the organism forward.3 Nevertheless, contractile tissue is definitely the most typical, powerful and dominant source of animal motility. Without it the large motile animals of the Cambrian and onward could not exist as motility by cilia comes with strong size and efficiency constraints that are only overcome by contractile tissue (Seipel and Schmid 2005). Muscle forms the animal’s ‘prime mover’ (Vogel 2003) and is the key feature of the standard sensorimotor organization of modern animals, constituting around 40 % of human body weight. The rise of muscle-based motility is unquestionably a key transition in animal evolution. The SBT proposes that contraction-based motility goes back to the very origins of nervous systems and that both are intrinsically related. The main claim is that this source of animal motility is more than an essentially arbitrary effector, contraction-based motility is central to nervous systems and the ASMO itself.

Following Pantin, the SBT stresses that contraction-based motility requires the integration of such contractions across the whole—or at least large parts of—the animal’s body. The SBT also emphasizes that an account of early nervous systems should derive from generic features that can be assumed to have been present in a Precambrian context and that could be utilized for this new purpose of coordination, such as the presence of electrically excitable cells, chemical signaling between cells and contractile cells. It also assumes an epithelial organization that, together with the extracellular matrix it creates, constitutes the fundamental building material of animals making up all their intricate forms and internal spaces (Holland 2011; Leys and Riesgo 2011). Like Pantin, the SBT stresses spontaneous activity within the organism, such as internal pacemakers (Passano 1963; Lichtneckert and Reichert 2007). Pantin himself acknowledged the presence of direct reflexes to specific stimuli, but thought of these as secondary developments that could only evolve and exist in the context of a whole acting organism, a position that is followed by the SBT. In all cases, the need for a functional understanding of how an elementary contraction-based motility mechanism might have worked and evolved is central.

At a neuronal level, the SBT differentiates between two essential properties of modern neurons: (a) Neurons have synapses that enable electrical signaling to other cells through the release of neurotransmitters. (b) Neurons have axodendritic processes that enable them to send and receive these signals to and from specific targets cells across long distances. While these two properties are combined in modern neurons, they may have evolved independently and at different times (Ryan and Grant 2009). As discussed above, the mechanisms for synaptic signaling, such as various parts of the postsynaptic scaffold, are already present in unicellular organisms and can be said to predate the axodendritic processes that require a multicellular context (ibid.). The question addressed is how protoneurons—defined as cells having (a) but not (b)—capable of synaptic signaling to neighboring cells could have been functional in a way that scaffolded the evolution of full neurons with axodendritic processes, that enabled signaling to non-neighboring cells.

The SBT conjectures that the evolution of the first nervous systems took place in two different phases. The first phase involved the evolution of excitable myoepithelia. These are epithelia that have both contractile properties (Mackie 1970; Lichtneckert and Reichert 2007) and conduct electrical activity across their surface (Josephson 1985). Such epithelia are both coordinator and effector at the same time. In contrast to modern forms of excitable myoepithelia, the SBT suggests that these early forms were constituted by protoneurons capable of chemical transmission through exocytosis, similar in outline to signaling by chemical synapses (Keijzer et al. 2013).4 Such a configuration would consist of an unbroken sheet of protonervous system tissue, each cell signaling to its immediate neighbors. This form of signaling is at heart similar to other forms of chemical signaling between cells and the molecular machinery involved is very old and can have been present at a very early date (Ryan and Grant 2009; Liebeskind et al. 2011). While this form of excitable myoepithelia is hypothetical at present, preliminary modeling studies indicate that such a set up could work as a mechanism for organizing patterned contractions across the epithelium (De Wiljes et al. 2010).

In a second phase, such a protonervous system would evolve a comparatively small number of more specialized signaling cells with elongated axodendritic processes by means of which those cells could send signals to nonadjacent cells across the epithelium. This would result in a diffusely connected nerve net, a nervous system that is spread out across the animal body with no or very little cephalization and generally considered as the most primitive form of nervous systems (e.g. Miller 2009; Moroz 2009). There are many possible reasons for initiating this second step, which range from minimizing metabolic costs, enabling more reliable signaling through connections that were not on the surface of the animal, and the ability to cross gaps between non-adjacent contractile tissues.

With the advent of nerve nets and the comparatively long distance connections provided by the neurons constituting them, the placement and form of both contractile surfaces and nervous systems can become much more variable. The contractile apparatus could eventually be cut loose from its placement on the animal surface and repositioned as internal muscle while remaining integrated by the long distance connections of the nerve net. Also, true neurons can themselves be repositioned within the body while their functioning is maintained through long distance connections. Clustering of neurons and cephalization subsequently becomes possible where main parts of a nervous system are repositioned within the animal body and separated from the contractile surface. From here on there is a route of general differentiation leading to complex nervous systems and animal bodies that we are all familiar with and which fits the input–output view so well.

Summarizing, the SBT constitutes a coordination view that outlines a gradual evolutionary change of functional coordinative structures that starts with excitable myoepithelia and progresses to full nerve nets composed of neurons. This skin brain scenario involves a reinterpretation of early nervous functioning that diverges from the idea that nervous systems at a fundamental level are a conductive or information processing system that is only connected to the world through its sensors that provide it with input and effectors that transduce internal processing into events that effect the environment as output. For both these connections, the SBT has a different story to tell and together these lead to the formulation of a specific animal sensorimotor organization that is shared by animals relying on contraction-based motility. The next two sections will develop this idea of a specific ASMO by discussing how the SBT deals with motility and sensing respectively.

The SBT claims that early nervous systems achieve motility in a way that is not suitably characterized as output. In this context, ‘output’ refers to the idea that a nervous system’s internal operation can be meaningfully dissociated from the behavior or activities that it initiates or controls. The classic notion of ‘motor control’ would provide an example where neural signals initiate and control motility (e.g. Orlovsky et al. 1999). In contrast, skin brains—taken here to include both myoepithelia and diffuse nerve nets—are conceptualized as physically intertwined with a contractile surface instead of constituting a separate controlling system. A second and deeper contrast concerns the foundational role of the contractile surface with respect to a skin brain organization. The latter is not an independently existing controlling system but an organization built in direct connection to a specific contractile tissue across which it helps to modulate electrical and contractile activity. Appreciating this point involves a mind switch away from a general agent-style interpretation of nervous system operation and towards a focus on the requirements imposed by the need to generate patterns of contraction and extension across a specific physical surface.

The starting point for the skin brain proposal is a contractile tissue that extends across a significant portion of the animal body. Patterns of contraction across this tissue will allow the organism to move in specific ways. The total contractile surface that an animal has available for motility will be referred to as an animal’s Pantin surface (Keijzer et al. 2013).5 For each animal species—and ultimately for each individual animal—this Pantin surface will have a specific size and shape. Muscle-based motility can then be conceptualized as deriving from the systematic patterning of contraction-extension across such a Pantin surface, which will be referred to as Pantin patterning. A simple example would be the coordinated contraction of the bell of a jellyfish. The functional result is that it propels water out of the central cavity, pushing the animal forward. Still, what the nervous system does is initiating a synchronized contraction across that particular jellyfish’s Pantin surface.

Thinking in terms of Pantin surfaces and Pantin patterning provides a useful way to generalize across the enormous variety of animal anatomies and to focus on what is common to all cases: Pantin patterning. Obviously, what outward behavior is actually produced will depend on the detailed morphology of individual animals and the environments they act upon, such as in the jellyfish example. However, the shift in perspective involved is that neural activity is not interpreted and described in terms of the perceptual and behavioral functionality that it enables, but as an organ—a tissue organization—that can induce intricate patterns of activation across its associated Pantin surface.

The point can be linked to Maturana and Varela’s (1980) influential differentiation between external organism-environment relations (structural coupling) and the local physiological operation of the organism (operational closure). The operation of nervous systems and the sensorimotor organization itself is not conceptualized in terms of external stimuli or the outwardly visible behavioral tasks that it enables. Instead, an account is provided of what nervous systems and their sensorimotor organizations do in which not the task or stimulus is held central but the animal itself. The concept of a behavioral task—e.g. feeding or mating—is not intrinsically tied to any particular kind of organism and assumes an agent that can execute this task (Keijzer 2006). As an analogy, understanding how a digital computer works should be held separate from the content of the specific programs or games that it runs. Similarly, Pantin patterning refers to happenings within particular animal organizations that can, and should be understood in their own right. At the same time, this organization constitutes the means by which functional behavior is achieved.

As a result, the conceptual question how early nervous systems may have functioned moves away from a focus on external circumstances—e.g. to what stimuli does the animal react—and towards understanding how various contractile organizations may have operated and how neural-like features may have enabled or changed various ways of operation. Such patterning is a major and general phenomenon in biology whenever specific biological shapes are produced, for example in animal morphogenesis. A Pantin surface constitutes a so-called excitable medium (Keijzer et al. 2013) across which excitatory and inhibitory activity can spread at various speeds producing large-scale patterns of contraction-extension by means of self-organization (e.g. Ball 2009; Goodwin 1994). How skin brains may specifically have contributed to patterning across this surface is a huge empirical question that is beyond this paper. Important ingredients are likely to be speed of activity spread, excitatory and inhibitory activity, jumping across areas by long-distance neural projections and the specific shape and size of the Pantin surface such that patterning can become harnessed and standardized in a way that is useful for contraction-based motility. The last point provides a key evolutionary link with developmental biology, as Pantin patterning can be presumed to require a standardized body—unlike for example fungi, plants and sponges—and constrained developmental processes that ensure such standardization. This link to developmental processes is likely to extend to the conceptual approaches provided by developmental biology (e.g. Levin 2011; Newman et al. 2006) as Pantin patterning can be seen as just another case of principles that are operating much more widely in animal organization.6

Summarizing, Pantin patterning is ill-described as output for various reasons. First, there is no dissociation between a controlling and a controlled system, there is simply a single contractile tissue with neural features incorporated or attached to it. Second, the Pantin surface is a physically circumscribed tissue with a particular size and shape that changes during individual development, growth, aging and damage. Patterning will be particular for that tissue and reflect the animal’s body rather than a generic output function that refers to a generalized functional behavior description, such as feeding or mating. Finally, Pantin patterning always involves a whole behaving organism acting as a unit. Again this diverges from the output notion, which can easily dissociate individual reflexes and stimulus reactions from the animal as a whole. I conclude that the skin brain proposal provides a way to characterize the mechanisms behind animal motility that diverges from the output side of the input–output view.

Pantin patterning provides the first half of an argument for an interpretation of the animal sensorimotor organization, ASMO, which diverges from the standard input–output view. Is there a second half to this argument or does the SBT still require the notion of ‘input’ to describe sensing as enabled by early skin brains? Sensing and sensitivity are used here according to a reading that Gibson described as “to detect something” and contrasted with “to have a sensation” (1966, p. 1). Sensing is here not used to refer to mental or intentional aspects of the notion of ‘sensing’. Sensing occurs when a specific environmental structure leads to a change in the organism that allows the organism to behave differently towards this environmental structure because of that change. I will argue that the strict organism-based way of casting this sensitivity by the SBT leads to a form of sensing that is not suitably described as input.

To start, it is important to stress that all living cells are sensitive to a wide variety of external chemical and physical features, which makes every cell capable of acting as some kind of sensor. Cellular sensitivity will also be present in the cells constituting nervous systems (Smith 2008; Greenspan 2007). The sensitivity of single cells can in certain cases be used by multicellular organisms to orient behavior without any nervous system (Leys and Degnan 2001; Nordström et al. 2003). However, the paradigmatic sensory device for animals with nervous systems is a multicellular spatially extended sensor array consisting of many parallel operating sensitive cells, with the retinal and skin surfaces as prominent examples (Gibson 1966). A single-cell sensor can signal the presence or intensity of an environmental feature—such as light—but sensor arrays enable organisms to become sensitive to patterns across extended surface arrays (Gibson 1966; Braitenberg 1984). It cannot be stressed enough how sensitivity to such macroscopic spatiotemporal structure of an environment is essential for the animal way of life. Without it the world of things, places and events that we and other animals inhabit would simply not be accessible. Given their central importance, the question here becomes: How did such sensor arrays and their neural infrastructure first evolve?

In Braitenberg’s illustration of the classic input–output view, sensor arrays derive from the evolutionary accumulation of spatially organized individual sensors into increasingly complex arrays and circuits geared to detect complex environmental features. Interestingly, such sensor arrays rely to a large extent on connections and interactions between cells within the array; that is to connections transverse to the input–output direction. As the importance of such transverse connections is well-established in neuroscience, one of the assets of the skin brain proposal is its focus on the evolution of a transverse nerve net organization spread out across the animal body. Such a nerve net organization provides a good precondition for the evolution of more specific sensor arrays—most notably related to touch—dispersed across the animal body. Given the general sensitivity of individual cells to environmental stimuli, one can envision how a skin brain organization incorporates cellular sensitivity to influence its patterning activity in ways that are generally beneficial for the organism, say in amount of food uptake. The transversely organized skin brain would be well-suited to combine patterns of stimulation across its surface because its main activity relates to organizing such patterning for motility.

This point becomes even stronger as soon one realizes that Precambrian animals must have been soft-bodied and eyeless (e.g. Dzik 2007; Parker 2003), conditions that preclude a stable physical platform for any sensor array. In contrast to vision with a comparatively small retina that can be stabilized, the epithelia of soft-bodied organisms are ongoing contracted and stretched, making a stable and precise configuration of tactile sensor cells challenging. This may seem problematic when it comes to providing stable and reliable input patterns, but these contractions and extensions are mostly self-induced and not random. Therefore, any such epithelial sensor array should not be considered as a passive and static sensor surface but rather as an active exploratory sensor device that actively interacts with its environment. This idea closely fits O’Regan and Noë’s sensorimotor theory of perception (2001; O’Regan 2011). They stress how self-initiated movements cause systematic and specific changes across sensory surfaces—what they call sensorimotor contingencies—to which an animal can become attuned (ibid.). Applied to the present case, endogenously produced Pantin patterning would lead to movements that change the sensor array in specific ways, which in turn would influence the skin brain and its patterning such that it compensates for and adapts to external disturbances of its ongoing activity. Sensing and moving are intrinsically tied together here.

The idea of a deep and intrinsic connection between sensing and moving is now widely established and specifically developed within embodied approaches to cognition (Hurley 2001; Chemero 2009; O’Regan and Noë 2001; O’Regan 2011). Embodied cognition stresses, in various ways, that the coupling between acting and sensing is the key to intelligence and distances itself from the notion of an internally situated ‘intelligent system’. The SBTs stress on the interweaving of contractile and sensory surfaces not only fits in with these embodied approaches but also adds new and more specific ideas concerning the basic organization of the animal sensorimotor organization and the intrinsic connection between moving and sensing here.

Embodied approaches stress the intrinsic connection between sensing and moving but so far did not yet apply this idea to the animal organization itself, taking organisms with extended sensor arrays and definite action capabilities as a starting point. The SBT highlights the problem how early multicellular organizations became sensitive to extended surface structure in the first place (Sheets-Johnstone 2011): What kind of tissue organization could first come to incorporate and use—and in that way sense—external spatial patterns given its own flabby constitution? How can surface structure become meaningful to a biological organization that is initially organized at a cellular and biomolecular level? A particular proximate organization is required that makes this incorporation possible. At this point, the SBT provides a radical idea: The body itself becomes a sensing device that is at heart independent of input or external sensors. A skin brain organization provides the means to allow an animal to differentiate between external surface structures in a way that does not build on sensory input as a precondition.

In a nut-shell, the SBT states that skin brains need to be sensitive to the internal Pantin patterns they generate; therefore the resulting embodiment will also become sensitive to environmental structure that impinges on this patterning and changes it. This sensitivity would be solely based on self-initiated movements and internal feedback derived from mechanical obstructions of the animal’s body and does not require sensors triggered by events outside the body. The basic idea is described by O’Shaughnessy (1989) in an intuitive way when he discusses the case of a blind man with a cane who should be able to probe his environment with this cane even without skin contact merely by muscle sense triggered by the resistance encountered with his cane.

Let’s unwrap the idea in some more detail. To induce motility through contraction, specific patterns of contraction-extension fitted to a particular Pantin surface are required to induce, for example, peristaltic movement across a worm’s body. While the Pantin surface is comparatively fixed and stable for any given animal—allowing standardization of patterning for separate species—it is not completely fixed. Various forms of variability at various time-scales are present, ranging from longer-term changes such as growth, short-term changes in stress and activity produced by the activation and movements themselves, and various features such as temperature, chemical changes and also damage and dysfunctions. As such inevitable variability could easily disturb global patterning—making it dysfunctional—skin brains must be sensitive to the ongoing Pantin patterning and counteract disturbances of functional contraction patterns.

To do this, skin brains must modify local cellular and biomolecular features in ways that modify global Pantin patterning such that functional movements are generated. As mentioned above, this requirement is highly similar to morphogenetic and regenerative processes during development where local activity is also dependent on its position within the global organization of the developing organism (Levin 2011, 2013). I will just assume for now that biomolecular and cell-level configurations can accomplish this task, one option being the use of stress-sensitive ion-channels that modify conduction characteristics (Gottlieb and Sachs 2012). In this case, the animal involved will become sensitive to the ongoing dynamical state of its own body: the global bodily distribution of contraction-extension at any particular moment in time. In a way this is a primitive form of proprioception but more basic and without specific muscle-based sensors. Such an arrangement binds the motile body of the animal into a unified dynamic whole that is sensitive to the ongoing dynamical contraction changes across this body and influencing the processes that generate and maintain these same patterns. The activity across—and thus within—the skin brain is directly sensitive to and reflecting the spatial lay-out of the animal body. Neural activity is at a deep level attuned to spatiotemporal structure at the bodily scale and intrinsically reflects this spatiotemporal structure. Because of their own activity as patterning devices, skin brains become sensitive to the spatiotemporal dynamics of their own extended bodies.

Given that a skin brain organization enables an organism to become sensitive to the dynamics of its own body, such sensitivity could—even must—extend to external surfaces that touch and impinge on this body. A skin brain organization is presumed to be present in simple, soft-bodied organisms, presumably small and crawling while in direct physical contact with the environmental substrate. For such an organism, sensitivity to the bodily dynamics of contraction-extension would also take in external disturbances in Pantin patterning when external surfaces impinge upon that body by either allowing or hindering body contractions or extensions (see Fig. 1). When the external substrate obstructs bodily movement, the animal would sense the obstruction as a disturbance of patterning within the Pantin surface even without any dedicated external sensor. Internal sensitivity suffices to generate a basic form of active touch (Gibson 1962; O’Shaughnessy 1989).

The sensor-less sensing body is an idealization, aimed to focus on the central idea that a skin brain organization turns the animal body itself into a new kind of multicellular organization that is capable of accessing and handling extended environmental surface structures such as shapes, textures and movements. Skin brains provide an organization that can become differentially sensitive to environmental features at a bodily scale because it must be already differentially sensitive to the spatial dynamics across its own Pantin surface. This internal bodily sensitivity provides the scaffold upon which a similar sensitivity to external spatial organization becomes possible.7 This direct linkage between internal and external structure provides the foundation of the specific animal sensorimotor organization, the ASMO.

The sensor-less case highlights the contrast with the input–output view as it provides a form of sensing without external sensors providing input. At the same time, bodily sensing does not diminish the importance of external sensor arrays. However, instead of watering down the ASMO concept, sensor arrays easily fit within the ASMO and augment it: Sensors do here not function as input devices as specified by the input–output view. Bodily sensing provides a fundamental example of systematic relations between self-initiated motion and feedback. Initially from the contractile surface itself, but from here on, the same principle can be used when motion-induced changes across external—or internal—sensor arrays feed back into nervous system activity resulting in various sensorimotor contingencies. Which contingencies would depend on the kind of energy the sensor arrays are sensitive to—e.g. pressure or electromagnetic waves. But such differences become superficial compared to the fact that the same principle of various sensorimotor contingencies applies to all, providing different ways of sensing that enable animals to orient themselves with respect to environmental surface structure.

Adding external sensors to the ASMO therefore does not imply a return to the input–output view. It actually strengthens the notion of an ASMO and makes it more versatile. An interesting implication is that while O’Regan and Noë’s original formulation of the sensorimotor theory focused on human vision and assumed the presence of sensors and effectors, the SBT provides the outlines of a foundation of a sensorimotor theory at a very early stage of nervous systems evolution, while making sensorimotor contingencies a crucial feature of animal sensing.

To summarize, sensing as accomplished by animals with skin brains is insufficiently described as ‘input’. Instead, the animal body itself becomes a sensing device through its use of contractile tissues and the environmental feedback this generates, both within and external to the body. Together, this constitutes a specific animal sensorimotor organization, or ASMO, that differs from the input–output view on both nervous system and the sensorimotor architecture of animals.

This paper aims to address a seemingly fundamental limitation of a specific coordination view on the origins of nervous systems: As the SBT emphasizes the evolutionary need to coordinate motility it seems to ignore the sensory aspects of early nervous systems. In response, I sketched how the SBT provides an account of moving and sensing. Instead of neglecting sensory issues, this coordination view provides a new account of sensing as enabled by early nervous systems: The skin brain organization provides a specific animal sensorimotor organization that differs from the input–output view’s interpretation of a sensorimotor organization.

A good way to highlight the differences in some detail is by returning to the eight typical features of the input–output view, derived from Braitenberg’s vehicles in “The input–output view on nervous systems and the animal sensorimotor organization” section, and to contrast them to their ASMO counterparts:

The ASMO operates in a way that is different from current artificial sensorimotor organizations;