Pharmacological evidence is consistent with a prominent role of spatial memory in complex navigation

Abstract

The ability to learn about the spatial environment plays an important role in navigation, migration, dispersal, and foraging. However, our understanding of both the role of cognition in the development of navigation strategies and the mechanisms underlying these strategies is limited. We tested the hypothesis that complex navigation is facilitated by spatial memory in a population of Chrysemys picta that navigate with extreme precision (+3.5 m) using specific routes that must be learned prior to age three. We used scopolamine, a muscarinic acetylcholine receptor antagonist, to manipulate the cognitive spatial abilities of free-living turtles during naturally occurring overland movements. Experienced adults treated with scopolamine diverted markedly from their precise navigation routes. Naive juveniles lacking experience (and memory) were not affected by scopolamine, and thereby served as controls for perceptual or non-spatial cognitive processes associated with navigation. Further, neither adult nor juvenile movement was affected by methylscopolamine, a form of scopolamine that does not cross the blood-brain barrier, a control for the peripheral effects of scopolamine. Together, these results are consistent with a role of spatial cognition in complex navigation and highlight a cellular mechanism that might underlie spatial cognition. Overall, our findings expand our understanding of the development of complex cognitive abilities of vertebrates and the neurological mechanisms of navigation.

Reptilian Cognition: A More Complex Picture via Integration of Neurological Mechanisms, Behavioral Constraints, and Evolutionary Context

“…Building on this study, we recently treated freely navigating painted turtles with scopolamine to determine if ACh facilitated migratory navigation. [98] Scopolamine disrupted the navigation ability of experienced adults, but not juveniles learning to navigate. We followed up this work by repeating the experiment with a specific M1 ACh receptor antagonist and found that blocking these receptors not only disrupted the recollection of spatial memories of migrating adults, but prevented naive turtles from forming such memories and learning migratory routes.…”

“…Treatment with scopolamine reduced maze learning compared to controls, demonstrating a role of ACh in spatial memory recall in painted turtles. Building on this study, we recently treated freely navigating painted turtles with scopolamine to determine if ACh facilitated migratory navigation . Scopolamine disrupted the navigation ability of experienced adults, but not juveniles learning to navigate.…”

“…[96,97] Furthermore, the effects of pharmacological treatments are often reversible, and often, rapidly so, allowing for more complex experimental designs relative to the neuroanatomical manipulations (e.g., lesions) discussed above. Finally, pharmacological manipulations can be easily done in the field of freeliving animals, [98,99] giving broad ecological and evolutionary relevance to the results of such experimentation. [100] Acetylcholine (ACh) influences aspects of learning and memory in mammals and birds.…”

Of molecules, memories and migration: M1 acetylcholine receptors facilitate spatial memory formation and recall during migratory navigation

“…Pharmacological manipulation with scopolamine, a general muscarinic acetylcholine receptor (AChR) antagonist, successfully blocks the formation and recall of spatial memories during laboratory experiments of navigation [ 14 , 16 – 18 ]. Moreover, scopolamine alters the precision of animal movements in the field during migration [ 19 , 20 ], supporting the role of the cholinergic system, and potentially spatial cognition, in large-scale migratory movements. Such studies have been critical to our understanding of how the brain produces spatially explicit memories, and how such memories influence navigation behaviours.…”

“…alterations in thirst, light sensitivity, and motivation) with a generalist antagonist (reviewed by Klinkenberg & Blokland [ 15 ]), it is possible that the disruptions in navigation observed during these migratory studies (e.g. [ 19 , 20 ]) could have resulted from the manipulation of non-spatial, non-cognitive processes such as sensation, perception, or attention. Thus, such studies could not definitively conclude that observed changes in navigation were solely due to a manipulation of spatial memory.…”