Figure 4 illustrates how the eumetazoan nerve nets evolved into the neural tube between 750 and 650 Mya. The legacy of the distinction between the ANS and BNS can still be found in cnidarians, such as jellyfish and anemones. In our lineage, the bilaterians, the body became elongated, stretching the blastopore into a slit, which then fused in the center to form a digestive tract. At one end of the body, the ANS and BNS merged (Arendt et al., 2016; Tosches & Arendt, 2013) into what would eventually become the head and a centralized brain—although only in a few lineages, such as arthropods, annelids, some mollusks, and chordates (Northcutt, 2012). The rest of the BNS remained on the ventral side of the body in protostomes (annelids, mollusks, arthropods, etc.), but in our branch, the deuterostomes, the body inverted such that the entire nervous system now became dorsally oriented and separate from the mouth and digestive tract (Holland, 2015; Lowe et al., 2006). Finally, in chordates, the nervous system folded inward into the body, forming what defines the basic neural plan to the present day (Nieuwenhuys & Puelles, 2016), as is shown in the inset of Fig. 4. That plan can be described as a tube that became progressively subdivided over evolutionary time, into “neuromeres” along its rostro-caudal axis, and into radial sectors, including “alar” regions near the roof plate and “basal” regions near the floor plate. In caudal regions, the alar and basal regions correspond, respectively, to the dorsal and ventral horns of the spinal cord, but at the rostral end the tube has become highly expanded and curved such that the topology is challenging to recognize in modern brains. Nevertheless, the fundamental morphological unit is still a radial sector defined by gene expression gradients, where cell proliferation occurs at the ventricular surface prior to migration (Nieuwenhuys & Puelles, 2016).

Fig. 4 Sequence of changes in early nervous systems leading to the basic plan of chordates. Evolutionary time along the lineage leading to vertebrates is indicated from left to right, with cnidarians (jellyfish, anemones, etc.) and protostomes (annelids, insects, mollusks, etc.) diverging along the way. The inset shows the basic organization of the chordate nervous system and its topological axes, based on Nieuwenhuys and Puelles (2016) Full size image

This dramatic sequence of events culminated in the common ancestor of all chordates, a worm-like creature that lived during the Ediacaran epoch (635–540 Mya) and is believed to have resembled the modern amphioxus (Bertrand & Escriva, 2011; Lacalli, 2001, 2008; Wicht & Lacalli, 2005). Its nervous system was a tube with two main regions (Albuixech-Crespo et al., 2017). The rostral end was the “archencephalon,” most of which was derived from the legacy of the merged ANS/BNS. It still contained the chemo- and photosensitive cells and still controlled the global behavioral state through hormonal secretions, and most of it would eventually become what we now call the hypothalamus. The rest of the neural tube was the “deuterencephalon,” which derived from the BNS. It still controlled oscillatory contractions and would eventually become the hindbrain and spinal cord.

Extensive studies of the amphioxus (Holland & Holland, 1999; Lacalli, 2001, 2004, 2008; Putnam et al., 2008; Shimeld & Holland, 2005; Wicht & Lacalli, 2005) and larval tunicates (Lacalli & Holland, 1998; Ryan, Lu, & Meinertzhagen, 2016) suggest that the central nervous system of early chordates primarily consisted of a rudimentary hypothalamus attached to a locomotor hindbrain and a spinal cord that implemented undulatory swimming. In addition to controlling bodily physiology, the hypothalamic region controlled temperature- and light-dependent circadian activity patterns and simple control of filter-feeding behavior. The latter function involved shifting locomotor patterns from local exploitation to long-range exploration, on the basis of the richness of nutrient state signaled by dopamine (Hills, 2006), as described above.

An additional behavior, visually guided escape, was governed by a group of neurons in the alar portion of the caudal end of the archencephalon (Lacalli, 2018b), derived from the BNS, which would eventually become the midbrain (Fig. 5A). These received excitatory input from a central patch of photosensitive cells at the rostral tip of the neural tube and projected ipsilaterally to a basal set of neurons that stimulated fast undulatory swimming. Because the photosensitive cells fired in response to a reduction of light, whenever a shadow fell on the animal it would rapidly swim away. Gene expression data suggest that this circuit, still seen in the amphioxus, is homologous to the tectum of vertebrates, its retinal input, and its output projection to locomotor regions (Lacalli, 1996, 2006, 2018b; Shimeld & Holland, 2005; Vopalensky et al., 2012). Note that the escape circuit, when viewed from the perspective of a control system, still obeys the basic scheme of negative feedback control. Here, the impetus is caused by external conditions—a shadow that stimulates the photosensitive patch—and the response is escape, which moves the animal until the shadow is gone.

Fig. 5 Evolution of avoidance and approach circuits. (A) Unfolded view of the neural tube of the putative last common ancestor of chordates. Escape behavior involved a single photosensitive patch of cells in the rostral tip, which projected bilaterally to the “tectum,” which projected ipsilaterally to basal “reticulospinal” neurons that controlled oscillatory locomotion. (B) In the cephalate, the eye patch split and moved to the lateral sides of the head, with contralateral projections to the tectum. (C) In early vertebrates, the eyes folded into cups, and the tectum differentiated to include a rostral region that projected contralaterally to the reticulospinal cells. This new circuit implemented visually guided orient-and-approach behavior. (D) In the presence of multiple threats (1 and 2), the averaging response (1 + 2) is effective in escaping from all of them. (E) Unlike escape, averaging between two stimuli for approach is maladaptive, making winner-take-all selection necessary. MHB, midbrain/hindbrain boundary; ZLI, zona limitans intrathalamica Full size image

Gradually, a distinction formed within the archencephalon, between the rostral regions controlling nutrient balance and more caudal regions controlling escape behavior, leading to two distinguishable developmental domains: the ANS/BNS-derived “prosencephalon” (left ends of the images in Figs. 5A–5C) and the BNS-derived “dimesencephalon” (mid regions, in a different color) separated by the future site of the zona limitans intrathalamica (Albuixech-Crespo et al., 2017), a major gene expression boundary in brain development. This provides an example of how a single sensorimotor system gradually differentiated into two distinct segments that took on different functional roles: foraging versus escape. Nevertheless, due to their shared history, they retain similarities that provide explanatory power. In particular, they lay the foundations for what will later become the two main systems for visually guided behavior: a retino-tectal circuit for spatial orientation, and a retino-telencephalic circuit for advanced foraging and interaction.

About 540 Mya, the world’s fauna underwent a dramatic increase in diversity, called the “Cambrian explosion,” partially driven by advances in predation (Bengtson, 2002; Erwin et al., 2011). The ancestors of early vertebrates survived these tumultuous times through two advances in sensorimotor behavior. First, in what Ann Butler has called the “cephalate” (Butler, 2000), the single central photosensitive patch split into two patches that migrated to the sides of the head (Fig. 5B). The initially balanced visual input to the tectum continued to drive escape behavior, but over time projection patterns that were contralaterally biased proved most useful. That is because if a shadow fell on the left eye patch, it stimulated activity in the right tectum, which projected ipsilaterally to the locomotor region, causing the animal to first turn to the right before swimming away, akin to the “vehicles” of Braitenberg (1984). Conversely, leftward escape was initiated by a shadow falling on the right. As the eye patches expanded, they folded into cups and formed a lens (Lamb, 2013), resulting in a two-dimensional retina that provided a topographic mapping of external stimuli. The tectum expanded in parallel, with a matched topographic map of space in its superficial layers and gradients of downstream projections in its deep layers. The result was an “action map” of oriented escape responses to threatening stimuli at specific locations in the external world.

Microstimulation studies have revealed the presence of an organized map of oriented escape responses in the tectum of lamprey (Saitoh, Ménard, & Grillner, 2007), a jawless fish whose ancestors diverged from ours about 520 Mya. Different sites of stimulation induce rapid swimming, struggling, as well as contractions that produce downward shifts of the eyes and head and C-shaped body bending—in short, the types of species-specific behaviors that lamprey use to escape threats.

Microstimulation has also revealed a region in the rostral part of the lamprey tectum that produces behavior orienting toward objects—including eye and head turning followed by swimming. Interestingly, this region of the tectum receives input from a part of the retina that is sensitive to space in front of the animal with a complex collection of retinal ganglion cells, and it projects mostly contralaterally to the spinal cord (Jones, Grillner, & Robertson, 2009; Kardamakis, Saitoh, & Grillner, 2015). In short, it implements approach behavior (Fig. 5C).

We can describe the resulting architecture of the early vertebrate brain as a set of tectal circuits for different types of species-typical behaviors, each implemented as a closed feedback loop with the world aimed at eliminating the condition (“impetus”) that motivates it. A threat on our left motivates turning right so that the threat is behind us; a threat behind us motivates forward locomotion until it is gone. A food item in front motivates approach until the food is ingested and consumed. In each case, something about the world specifies an opportunity or a demand for action—what Gibson (1979) called an “affordance.” The neural activity in the circuit responding to that affordance is not a representation of a thing in the world; it is the specification of an action to take within the world. We can call it a “pragmatic representation” of action, as opposed to a “descriptive representation” of explicit knowledge (Cisek & Kalaska, 2010).

The presence of both approach and avoidance circuits raises the issue of behavioral selection: Given some stimulus in front of it, should the animal approach or escape? In lamprey (as in many vertebrates), that selection is performed within the tectum itself. For example, a small stimulus excites the cells involved in approach, which have a low threshold, but large looming stimuli excite the high-threshold cells that initiate escape (Kardamakis et al., 2015). More finely tuned selection could involve the detection of what ethologists call “key stimuli”—a set of specific cues that motivate a given action (Hinde, 1966). For example, frogs famously possess tectal “bug detectors” that combine converging information from specialized retinal cells sensitive to local sharp edges, dark spots with high curvature, fast motion signals, and local dimming (Lettvin, Maturana, McCulloch, & Pitts, 1959). In mammals, more sophisticated arbitration between approach and avoidance behavior is governed by descending modulation from the basal ganglia (Hormigo, Vega-Flores, & Castro-Alamancos, 2016).

In addition to the selection between approach and avoidance, a different type of selection is necessary within the approach system. Consider what happens when multiple stimuli are present simultaneously. If either or both of these are considered threats, then escape behavior is necessary, and in this case an average response is effective (Fig. 5D). However, that is not the case for approach, in which the average response would miss both targets. In this scenario, what is needed is a winner-take-all selection, whereby one response completely suppresses the other. This can be accomplished through lateral inhibition (Grossberg, 1973), a mechanism that can indeed be found in the lamprey tectum (Kardamakis et al., 2015).

To summarize, the lamprey tectum appears to contain the circuits for two kinds of spatially oriented behavior, which can broadly be described as “approach” and “avoidance.” Both receive contralateral input from the eyes, as in the ancestral cephalate. However, while the avoidance system retains the ancestral uncrossed output projections, in the approach system these projections are crossed. Importantly, these two systems appear to have been retained throughout vertebrate evolution. For example, in fish, stimulation of the optic tectum elicits eye movements and body bending, followed by several tail beats, whose orientation is either contraversive or ipsiversive, depending on the site of stimulation and current strength (Herrero, Rodriguez, Salas, & Torres, 1998). In rodents, stimulation of the superior colliculus (SC)—the mammalian homologue of the optic tectum—produces approach or avoidance actions through two distinct circuits (Comoli et al., 2012; Dean, Redgrave, Sahibzada, & Tsuji, 1986; Sahibzada, Dean, & Redgrave, 1986). Stimulation of the medial SC, which receives visual information from space above the animal and projects ipsilaterally to the brainstem and spinal cord, elicits defensive and avoidance actions. Stimulation of the lateral SC, which receives visual information from lower visual space as well as the vibrissae and projects contralaterally, elicits approach and appetitive behavior. This makes good sense in the world of rodents, in which predators often approach from above and food sources are found low to the ground. A similar distinction has also been found in the SC of primates. It is well known that the SC is implicated in the control of gaze and body orientation through contralateral projections to the brainstem (Basso & May, 2017), but its role in defensive behavior has only recently been demonstrated. In particular, chemical activation of the deep layers of the macaque SC evokes a dramatic increase in species-typical defensive behaviors, including cowering, escape, vocalization, and threatening gestures (DesJardin et al., 2013).

Alongside the elaboration of tectal visuomotor circuits of approach and avoidance, a second major advance in behavior during the early Cambrian epoch involved the elaboration of olfactory foraging systems. These originated in the rostral segment of the neural tube and involved the expansion of an olfactory region in the “alar” sector of the hypothalamus into what would ultimately become the telencephalon (Puelles, Harrison, Paxinos, & Watson, 2013). As we noted above in Fig. 3B, this ANS-related circuit was originally concerned with the control of nutrient concentration by arbitrating between local exploitation in nutrient-rich regions and long-range exploration away from nutrient-poor regions, governed by levels of dopamine (Hills, 2006), through its projections to “basal” locomotor centers. With advances in external chemical sensing, it was now possible to evaluate the nutrient environment before actual ingestion, and to use this to differentially bias actions. The early telencephalon was subdivided into two regions: the “pallium,” which implemented different olfactomotor actions (Derjean et al., 2010), and the “subpallium,” which arbitrated between them in the context of expected rewards (Redgrave, Prescott, & Gurney, 1999; Wickens & Arbuthnott, 2010). These regions would form the foundations from which the rest of the forebrain evolved. The subpallium became the striatum and pallidum of the basal ganglia, whose circuits are present in lamprey in all the detail so far studied (Grillner, Hellgren, Ménard, Saitoh, & Wikström, 2005; Robertson et al., 2014).

The differing demands of local exploitation versus long-range exploration led to the emergence of a distinction within the pallium between a ventrolateral sector (VLPall) that was specialized for exploitation and a medial sector (MPall) that was specialized for exploration. The ventrolateral sector used olfactory and gustatory signals, along with visual “key stimuli” arriving from the tectum via the “collothalamic” pathway (Butler, 2008), to guide appetitive approach actions, and would ultimately become the olfactory bulb, the insula, and piriform cortex. The medial sector, in contrast, used olfactory signals and direct “lemnothalamic” visual input (Butler, 2008) to guide navigation (Jacobs, 2012), and would eventually become the hippocampus (Jacobs & Schenk, 2003; Puelles et al., 2013).

Interestingly, part of the ventrolateral pallium of lamprey includes a retinotopic visual area and somatotopic areas receiving input from spinal and trigeminal systems (Suryanarayana, Pérez-Fernáandez, Wallén, Robertson, & Grillner, 2018), as well as a motor area from which microstimulation can evoke a rich repertoire of actions (Ocana et al., 2015). It is therefore topologically similar to the dorsal pallium (DPall) of jawed vertebrates, which is the homologue of the mammalian cerebral cortex (Butler & Hodos, 2005; Medina & Reiner, 2000). Although the similarity of these sensorimotor regions of the lamprey pallium to the mammalian cerebral cortex could be a product of convergent evolution, their detailed connectivity, synaptic properties, dendritic spine distribution, and neurotransmitters suggest they are a legacy of a circuit that existed in our last common ancestor (Ocana et al., 2015).

To summarize, at the root of the vertebrate phylogenetic tree, the nervous system consisted of a tube divided into rostro-caudal neuromeres, as is shown in Fig. 6 on the basis of the prosomeric model of Luis Puelles and colleagues (Puelles et al., 2013; Puelles & Rubenstein, 2003). The most rostral neuromere was the top-level controller, influencing bodily physiology through secretions of hormones to the rest of the body, and behavior through neuromodulation of the rest of the neural tube. This became what Puelles et al. (2013; Puelles & Rubenstein, 2003) call the “terminal hypothalamus” (THy in the figure). The next segment, called the “peduncular hypothalamus” (PHy in the figure), was the top-level controller of simple foraging behaviors. It included what would become the lateral hypothalamic area and an expanded alar portion called the telencephalon. The latter part consisted of a ventrolateral pallial sector concerned with olfaction and ingestion (the future piriform cortex and insula), and a medial pallial sector concerned with navigation (the future hippocampus), orchestrated through an underlying subpallial system (basal ganglia) that arbitrated between different kinds of behaviors. These telencephalic systems implemented a set of parallel sensorimotor loops that received input through the thalamus (with the exception of direct olfactory input) and effected output through basal descending pathways to more caudal segments. The caudal segments included the midbrain, including the tectal approach and avoidance circuits, as well as the hindbrain and spinal cord, which implemented the control of undulatory locomotion.

Fig. 6 Sagittal view of the basic organization of the ancestral vertebrate brain. Here, the neural tube is color-coded according to its major subdivisions: prosencephalon, dimesencephalon, rhombencephalon, and spinal cord. The alar portion of the second segment of the prosencephalon (PHy) expands into the telencephalon, in which additional domains can now be distinguished. These include subpallial sectors (striatum and pallidum) and pallial sectors (ventrolateral and medial). The putative future site of the dorsal pallium is marked as a subregion of the ventrolateral pallium. Only a few of the major pathways are shown, emphasizing how visual and olfactory information (blue lines, in online color figure) is used to guide tectal approach and avoidance behaviors (purple lines), and telencephalic foraging behaviors (green lines), arbitrated by modulatory pathways from the subpallium (red dotted lines). OB, olfactory bulb; PHy, peduncular hypothalamus; SNr, substantia nigra reticulata; THy, terminal hypothalamus Full size image

The early vertebrate nervous system described above, which was present half a billion years ago, contained almost all of the basic pieces of mammalian brains, as well as their gross topological organization (Ocana et al., 2015; Robertson et al., 2014). One major innovation occurred between 500 and 450 Mya, with the elaboration of the alar hindbrain into what would become the cerebellum (Bell, Han, & Sawtell, 2008). Other major innovations occurred as vertebrates emerged onto land about 400 Mya (Lu et al., 2012), including the elaboration of the swim bladder into lungs, transformation of fins into legs, and development of the circuits controlling terrestrial locomotion. The complexity of life on land opened up many new opportunities and demands and encouraged a vast expansion of the behavioral repertoire. This included some elaboration of the retino-tectal circuits, but even more significant advances occurred through differentiation of the sensorimotor circuits lying at the border between the ventrolateral and medial pallia. This region became the dorsal pallium of amniotes, and eventually gave rise to what in mammals would become the cerebral cortex.

It is difficult to know why the dorsal pallium took on such a major role in the evolution of mammalian brains (Aboitiz, Morales, & Montiel, 2003). One reason might have to do with the nocturnal lifestyle of the early mammals, which reduced their dependence of vision and emphasized olfactory-driven foraging, thus motivating elaborations of the olfactory telencephalon. Another key factor may have been the nature of sensory projections from the thalamus, which enter the dorsal pallium of sauropsids (birds and reptiles) tangentially, whereas in mammals they enter radially, forming columns that can be duplicated and repeated without incurring major connectivity costs (Striedter, 2005). Thus, the dorsal pallium of mammals could grow dramatically into what we now call the neocortex, with each portion maintaining its ancestral connections with sensory input, descending output, and recurrent loops with the basal ganglia and cerebellum. The existing architecture of parallel sensorimotor streams, each specialized for one aspect of the animal’s behavioral repertoire, could be expanded and parcellated to support a wider range of behaviors. For example, in the context of foraging, local exploitation could expand from simple types of approach and ingestion behaviors to a great variety of sniffing, burrowing, reaching, and grasping behaviors.

Figure 7 shows an unfolded and flattened topological map of the mammalian brain, still respecting the major subdivisions of the ancient neural tube. Here we see how the neocortex lies within the dorsal pallial sector of the expanded alar subregion of the peduncular hypothalamus. Although it is unfamiliar to think of the cerebral cortex as a subregion of part of the hypothalamus, this topological placement reflects its role within the functional hierarchy of behavior: (1) The hypothalamus is the top-level controller of the general state of the organism. (2) Its second, “peduncular” segment PHy specializes in the kind of control that extends through the environment by means of downstream projections to the rest of the nervous system. (3) The alar portion of that segment specializes in the guidance of foraging, ranging from local exploitation via olfaction/ingestion (ventral and lateral pallium) to long-range exploration (medial pallium, a.k.a. hippocampus), with all the sensorimotor interactions in between (dorsal pallium). (4) With the expansion of opportunities for sensorimotor interaction afforded by the terrestrial world, this last part of the brain has expanded massively, especially in mammals, to form a neocortex consisting of multiple parallel sensorimotor streams.

Fig. 7 Schematic organization of the mammalian brain, based on Puelles et al. (2013). Here, the dorsal pallium (neocortex) has been divided into the spatially topographic (light) versus nontopographic (dark) neocortical sheets (Finlay & Uchiyama, 2015) and superimposed with labels based on the cortical flat map of Swanson (2000). Within the neocortical regions, blue arrows (see online color figure) indicate processes specifying potential actions, while red arrows indicate information related to their selection. Note the topological similarity of the tectal and telencephalic sensorimotor circuits to those shown in Fig. 6. OB, olfactory bulb; MHB, midbrain/hindbrain boundary; PHy, peduncular hypothalamus; SNc, substantia nigra compacta; SNr, substantia nigra reticulata; THy, terminal hypothalamus; VTA, ventral tegmental area; ZLI, zona limitans intrathalamica Full size image

In all mammals, the neocortex consists of two sheets (Finlay & Uchiyama, 2015), a dorsomedial sector that is spatially topographic and a ventrolateral sector that is nontopographic (see the green shaded areas in the online version of Fig. 7). In primates, the former includes dorsolateral prefrontal cortex, cingulate regions, all of premotor, motor, sensorimotor, and parietal cortex, as well as retrosplenial cortex. The latter includes orbitofrontal, gustatory, and visceral cortex, limbic cortex, and the temporal lobe. Much of the dorsomedial neocortex is organized into what Michael Graziano has called “action maps,” a set of fronto-parietal circuits dedicated to different classes of species-typical actions (Graziano, 2016; Kaas & Stepniewska, 2016). In early mammals (300 Mya), this was probably quite limited and consisted simply of medial circuits concerned with locomotion and lateral circuits concerned with head and mouth movements (Kaas, 2017). Each of these circuits processed sensory information in an idiosyncratic manner specialized for its specific type of action (e.g., space near the legs for locomotion, space near the snout for ingestion), and each projected to a specific set of relevant effectors. Meanwhile, the ventrolateral neocortex processed information relevant to selecting the type of action that would be most relevant at a given time (Cisek, 2007). This included interoceptive signals about the current physiological state, relayed via the insula, as well as simple mechanisms for detecting “key stimuli” (Hinde, 1966), similar to those already found in tectal circuits.

The ideas above are closely related to the “affordance competition hypothesis” (Cisek, 2007; Cisek & Kalaska, 2010; Pezzulo & Cisek, 2016), which suggests that the cortical control of behavior involves the parallel specification of different action opportunities currently available in the immediate environment and a competition between them that is biased by a variety of factors, such as object identity, expected rewards, and current behavioral context. That hypothesis, strongly inspired by the “two visual systems” view of Milner and Goodale (Goodale & Milner, 1992; Milner & Goodale, 1995), proposes that the specification of potential actions occurs in sensorimotor cortex (dorsal visual stream, dorsomedial cortical sheet) as a biased competition (Grossberg, 1973) within a recurrent network composed of groups of cells “voting” for different actions. The selection factors that influence that competition come from the basal ganglia and frontal regions using information from temporal cortex (ventral visual stream, ventrolateral cortical sheet). The present framework of the more fundamental organization of behavioral control systems provides a context within which that hypothesis naturally fits, but it also motivates some important modifications, as described below.

As the behavioral repertoire of mammals continued to expand, so did the dorsomedial neocortex, and there was a differentiation and specialization of action-specific maps of sensory space. In primates, the expansion of parietal cortex was particularly dramatic, yielding a variety of idiosyncratic representations of space particular to the needs of different action types (Andersen, Snyder, Bradley, & Xing, 1997; Stein, 1992). For example, visually guided reaching actions involve medial intraparietal cortex (Cui & Andersen, 2011; Kalaska, 1996), which represents targets within reach with respect to the direction of gaze and the position of the hand (Buneo, Jarvis, Batista, & Andersen, 2002; Gallivan, Cavina-Pratesi, & Culham, 2009) and is interconnected with the frontal regions controlling reaching, such as dorsal premotor cortex (Johnson, Ferraina, Bianchi, & Caminiti, 1996; Wise, Boussaoud, Johnson, & Caminiti, 1997). Grasp control involves the anterior parietal area (Baumann, Fluet, & Scherberger, 2009), which is sensitive to object shape and is interconnected with grasp-related frontal regions such as the ventral premotor cortex (Nakamura et al., 2001; Rizzolatti & Luppino, 2001). The control of gaze involves the lateral intraparietal area (Snyder, Batista, & Andersen, 2000), which represents space in a retinotopic frame (Colby & Duhamel, 1996; Snyder, Grieve, Brotchie, & Andersen, 1998) and is interconnected with frontal regions controlling gaze and with the superior colliculus (Paré & Wurtz, 2001).

The ventrolateral neocortex expanded also, particularly its caudal portion, where nonegocentric visual information was processed. In primates, this grew so much that the entire cortical hemisphere bent around the insula, eventually forming the familiar curled shape of the human brain. Those temporal regions, originally concerned with simple “key stimulus” detection, became elaborated into more sophisticated mechanisms sensitive to behaviorally relevant classes of objects in the world. Computationally, object recognition has been described as the “untangling” of low-level features into a high-dimensional space in which meaningful categories of external objects are more readily separable (DiCarlo & Cox, 2007). This need not end at the temporal lobe, however. What selection of behavior really needs is not representations of objects per se, but classification of the relative subjective value of engaging with those objects, as a function of the animal’s current state. That is, the ancestrally most relevant category is not “apple,” but “edible item,” perhaps contextually modulated by the current context of hunger, thirst, fatigue, and so forth. In other words, what behavior needs is cues that help prioritize one action over another. Yoo and Hayden (2018) proposed that the kind of untangling proposed to explain object recognition can be postulated to continue into orbitofrontal regions, which are often associated with representations of economic value (Padoa-Schioppa & Assad, 2006). This notion is compatible with the observation that orbitofrontal cortex indeed lies at the rostral end of that same ventrolateral neocortical sheet that starts with nonegocentric visual (and auditory) processing (Finlay & Uchiyama, 2015).

The resulting sketch of the organization of the cerebral cortex is consistent with the idea of affordance competition, but it suggests a more specific proposal on the division of labor between different kinds of selection problems (Cisek & Thura, 2018). One type of decision that an animal must make is what aspect of its behavioral repertoire should be engaged at a given moment. For example, if a desirable fruit is within reach, then one can engage the reaching system to grab it and bring it to the mouth, but if it is out of reach, then one must first engage locomotion. In each of these cases, the affordance is specified by visual information about the geometrical relationships between body effectors and the objects around them, the cues for selection are provided by visual information about shape and color, and the consequences of each candidate action are predictable due to the reliability of interactions with the environment, which in some cases (e.g., locomotion toward a fruit) will make a new affordance available (Pezzulo & Cisek, 2016). The first task for an animal is to selectively activate one of its fronto-parietal systems (Graziano, 2016), the one dedicated to the type of action that is called for (e.g., reach or walk). This type of “between-system” selection could be driven by the basal ganglia, given their anatomical placement as a central hub from the very origins of telencephalic sensorimotor control (Grillner & Robertson, 2015; Redgrave et al., 1999). However, once that type of selection is made, there is still a “within-system” competition that must be resolved—for example, between different fruits that could be grasped or different foot placements that are possible. This kind of selection is different: It requires a map of actions, in a continuous and idiosyncratic space specific to each type of action (hand-centered reachable space for reaching, retinotopic space for gaze, etc.)—that is, within each of the fronto-parietal action systems. For example, once reaching is chosen, specification of different targets for reaching could take place within a population of tuned cortical neurons in the fronto-parietal reaching system (MIP, PMd, M1), which implement a “desirability density function” across the space of reaching actions (Pezzulo & Cisek, 2016), and the competition could play out across that population simply through lateral interactions (Cisek, 2006; Grossberg, 1973). Several lines of evidence suggest that when choosing specific actions within a given class of actions, it is the cortex that makes the choice (Klaes, Westendorff, Chakrabarti, & Gail, 2011; Pastor-Bernier & Cisek, 2011; Thura & Cisek, 2014), not the basal ganglia (Arimura, Nakayama, Yamagata, Tanji, & Hoshi, 2013; Thura & Cisek, 2017; Turner & Desmurget, 2010).

The resulting functional architecture at which we have arrived is still fundamentally based on feedback control (Ashby, 1965; Cisek, 1999; Powers, 1973), whereby interaction with the world is aimed at exploiting available opportunities (“affordances”) that reliably reduce or eliminate some deviation from a desirable state (“impetus”). These feedback interactions exist on many hierarchical levels. Some are concrete actions, and because many are present simultaneously, selection must be made both between different types of actions (Cisek & Thura, 2018) and within specific movements of a given type (Cisek, 2007). These “low-level” control systems themselves make possible new domains of interaction, such that complex behavior can be constructed upon a scaffolding of simpler behaviors (Pezzulo & Cisek, 2016), extending even into social interactions (Hendriks-Jansen, 1996). For example, if you can predict how other animals will respond to your actions, you can extend your control through them. This can be used to explain a variety of social behaviors, from the threat postures of monkeys to a baby’s interactions with its mother. The concept of affordances can even be extended to a cultural domain (Ramstead, Veissiere, & Kirmayer, 2016), and within that context can provide much-needed grounding for theories of meaning in linguistic communication (Cisek, 1999). In short, it is possible, at least in principle, to extend the basic sketch of the functional architecture of simple sensorimotor control to the more abstract domains that characterize human behavior, as was proposed long ago by Piaget (1954). Exploring those possibilities, however, is beyond the scope of the present article.