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. 2019 Oct;81(7):2265-2287.
doi: 10.3758/s13414-019-01760-1.

Resynthesizing behavior through phylogenetic refinement

Paul Cisek  1
Affiliations

Resynthesizing behavior through phylogenetic refinement

Paul Cisek. Atten Percept Psychophys. 2019 Oct.

Abstract

This article proposes that biologically plausible theories of behavior can be constructed by following a method of "phylogenetic refinement," whereby they are progressively elaborated from simple to complex according to phylogenetic data on the sequence of changes that occurred over the course of evolution. It is argued that sufficient data exist to make this approach possible, and that the result can more effectively delineate the true biological categories of neurophysiological mechanisms than do approaches based on definitions of putative functions inherited from psychological traditions. As an example, the approach is used to sketch a theoretical framework of how basic feedback control of interaction with the world was elaborated during vertebrate evolution, to give rise to the functional architecture of the mammalian brain. The results provide a conceptual taxonomy of mechanisms that naturally map to neurophysiological and neuroanatomical data and that offer a context for defining putative functions that, it is argued, are better grounded in biology than are some of the traditional concepts of cognitive science.

Keywords: Animal cognition; Cognitive neuroscience; Evolution; Neural mechanisms.

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Figures

Fig. 1
Fig. 1
Partial sketch of a conceptual taxonomy implicit in mainstream cognitive science and neuroscience
Fig. 2
Fig. 2
Phylogenetic tree of animals, emphasizing the lineage that led to humans. Branch points represent some of the divergences between different lineages, with timing estimated using molecular-clock analyses (Erwin et al., ; Wray, 2015). Thick lines indicate the presence of relevant fossil data (https://paleobiodb.org). Small rectangles indicate the latest estimated timing of the innovations described in the boxes. Many branch points and lineages are omitted for clarity. The silhouettes of example species are from http://phylopic.org. Note that the arrangement of the branches in the vertical direction is completely arbitrary. Here it is arranged so as to leave room to emphasize branch points and innovations along the lineage leading to humans, and this is the only reason for the apparent “Scala Naturae” of species along the right edge. ANS, apical nervous system; BNS, blastoporal nervous system; DPall, dorsal pallium; MPall, medial pallium; LPall, lateral pallium; VLPall, ventrolateral pallium; VPall, ventral pallium
Fig. 3
Fig. 3
Schematic behavioral control systems. (A) When the current nutrient state deviates from a desired state, locomotion is initiated, ultimately bringing the animal to a more desirable state. (B) Elaboration of nutrient state control into a high-level controller (ANS) and a lower-level controller (BNS) capable of two modes of locomotion, local exploitation, and long-range exploration. 5HT, serotonin; ANS/BNS, apical/blastoporal nervous system; DA, dopamine; NPY, neuropeptide Y
Fig. 4
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)
Fig. 5
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
Fig. 6
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
Fig. 7
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
Fig. 8
Fig. 8
An alternative conceptual taxonomy resulting from following a phylogenetic approach along the vertebrate lineage. Here, each functional category is conceived as a particular specialization of the functional category above it, and each corresponds to a biological structure that emerged as a specialization within an ancestral structure. AIP, anterior intraparietal area; CMA, cingulate motor area; FEF, frontal eye fields; LIP, lateral intraparietal area; MIP, medial intraparietal area; PMd, dorsal premotor cortex; PMv, ventral premotor cortex; SMA, supplemental motor area; VIP, ventral intraparietal area
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