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

Abstract

Many animals use complex cognitive processes, including the formation and recall of memories, for successful navigation. However, the developmental and neurological processes underlying these cognitive aspects of navigation are poorly understood. To address the importance of the formation and recollection of memories during navigation, we pharmacologically manipulated turtles (Chrysemys picta) that navigate long distances using precise, complex paths learned during a juvenile critical period. We treated freely navigating turtles both within and outside of their critical learning period with a specific M1 acetylcholine receptor antagonist, a drug known to disrupt spatial cognition. Experienced adult turtles lost all navigational ability under the influence of the drug, while naive juveniles navigated successfully. We retested these same juveniles the following year (after they had passed their critical period). The juveniles that initially navigated successfully under the influence of the antagonist (but were unable to form spatial memories) were unable to do so subsequently. However, the control animals (who had the opportunity to form memories previously) exhibited typical navigational precision. These results suggest that the formation of spatial memories for navigation occur during a critical period, and successful navigation after the critical period is dependent upon the recall of such memories.

A potential entanglement between the spinal cord and hippocampus: Theta rhythm correlates with neurogenesis deficiency following spinal cord injury in male rats

“…The power of theta rhythm significantly reduces in NMDA ablated or blocked animals, and their function is impaired in terms of spatial navigation and memory (de Oliveira Cabral, 2014; Korotkova, Fuchs, Ponomarenko, von Engelhardt, & Monyer, 2010). Besides NMDA, M1 receptors are extremely expressed and active in the hippocampus so that their inhibition interrupts encoding of memory in the spatial navigation tasks (Dennis et al., 2015; Leaderbrand et al., 2016; Roth & Krochmal, 2018). These receptors can be stimulated by recurring inputs, especially from the medial septum‐diagonal band of Broca.…”

“…GABAergic interneurons of the CA1 provide inhibitory feedback to local pyramidal neurons. This modulatory function is vital for the generation and synchronization of theta rhythm (Leaderbrand et al., 2016; Roth & Krochmal, 2018). The downregulation of GABAA receptor's expression alongside other receptors further contributes to the decline in the theta power.…”

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

“…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. [99] Pharmacological manipulation of other neurotransmitters and neuromodulators shows similar patterns. For example, given the role of N-methyl-D-aspartate (NMDA) in memory consolidation and long-term potentiation in mammals, [101] Avigan and Powers [39] experimentally manipulated NMDA in painted turtles that had been previously trained on an X-maze.…”

“…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 …”

“…[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.…”