4Other than formerly land-based mammals such as whales and dolphins that 5 have returned to an aquatic existence, it is uncontroversial that land animals 6 have developed more elaborated cognitive abilities than aquatic animals. Yet 7 there is no apparent a-priori reason for this to be the case. A key cognitive 8 faculty is the ability to plan. Here we provide evidence that in a dynamic 9 visually-guided behavior of crucial evolutionary importance, prey evading a 10 predator, planning provides a significant advantage over habit-based action 11 selection, but only on land. This advantage is dependent on the massive in-12 crease in visual range and spatial complexity that greeted the first vertebrates 13 to view the world above the waterline 380 million years ago. Our results have 14 implications for understanding the evolutionary basis of the limited ability of 15 animals, including humans, to think ahead to meet slowly looming and distant 16 threats, toward a neuroscience of sustainability. 17 Introduction 18The emergence of vertebrates on to land over 350 million years ago was preceded by a massive 19 increase in visual range when their eyes moved to the top of the head to look over the water 20 surface and tripled in size (1). The optical difference between inland waters-where transitional 21 tetrapods are thought to have emerged-and air resulted in more than a 100-fold increase in 22 visual range, from about a body length to hundreds of body lengths ahead (1, 2). Within the 23 greatly enhanced range of Devonian aerial vision was rich structure provided by vegetation 24 (3) and other terrestrial features, providing complex visual scenes to animals (Supplementary 25 Fig. 1A-B). In this study we will test the hypothesis that for visually guided behaviors, the 26 2 increase in visual range and observed environmental complexity that accompanied the onset of 27 terrestriality advantaged the evolution of neural circuitry for deliberation over multiple futures 28 (4, 5).
29This study builds on investigations into the neural basis of action selection that suggest the ex-30 istence of two competing, distinct, and largely parallel decision making systems: habit-based 31 action selection, and plan-based action selection (6, 7). These two control paradigms have 32 primarily been associated with the lateral striatum and its dopaminergic afferents (8-10) for 33 habit, and the interaction between hippocampus and the prefrontal cortex (nidopallium cau-34 dolaterale in birds (11)) (12-19) for planning. The similarity between lamprey (jawless fish 35 that preceeded mammals by 560 million years) and mammalian basal ganglia in the direct and 36 indirect pathways of the dopamine expressing striatal projection neurons (20-22) suggests that 37 this structure-and thus the habit-based action selection system it supports-evolved very early 38 on in vertebrate evolution. 39 In mammals, planning has been related to the phenomenon of nonlocal spatial representations 40 in hippocampal activity. Two quintessential examples of this phen...