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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.

SUBMITTER: Roth TC

PROVIDER: S-EPMC6253372 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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

Roth Timothy C TC Krochmal Aaron R AR

Proceedings. Biological sciences 20181114 1891

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 (<i>Chrysemys picta</i>) that navigate long distances using precise, complex paths learned during a juvenile critical per ...[more]

PMID: 30429306

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Project description:Ensembles of principal neurons in the basolateral amygdala (BLA) generate the initial engrams for fear memories, while projections from the BLA to the medial prefrontal cortex (mPFC) are essential for the encoding, transfer and storage of remote fear memories. We tested the effects of chronic pain on remote fear memories in mice. Male mice underwent classic fear conditioning by pairing a single tone (conditional stimulus, CS) with a single electric foot shock (unconditional stimulus, US). Sciatic nerve constriction was used to induce neuropathic pain at various time points before or after the fear conditioning. The mice with sciatic nerve cuffs implanted 48 h after the fear conditioning showed an increased freezing response to CS when compared to mice without cuffs or when compared to mice in which the nerve cuffing was performed 48 h before the fear conditioning. The enhancing effect of pain on consolidated fear memory was further tested and mice in which the nerve cuffing was performed 14 days after the fear conditioning also showed an increased fear response when tested 56 days later. We used immunostaining to detect morphological changes in the BLA that could suggest a mechanism for the observed increase in fear response. We found an increased number of calbindin/parvalbumin positive neurons in the BLA and increased perisomatic density of GAD65 on projection neurons that connect BLA to mPFC in mice with nerve cuffs. Despite the strong increase of c-Fos expression in BLA and mPFC that was induced by fear recall, neither the BLA to mPFC nor the mPFC to BLA projection neurons were activated in mice with nerve cuffs. Furthermore, non-injured mice had an increased fear response when BLA to mPFC projections were inhibited by a chemogenetic method. In conclusion, this study provides evidence that persistent pain has a significant impact on consolidated fear memories. Very likely the underlying mechanism for this phenomenon is increased inhibitory input onto the BLA to mPFC projection neurons, possibly from neurons with induced parvalbumin expression. Conceivably, the increased fear response to consolidated fear memory is a harbinger for the later development of anxiety and depression symptoms associated with chronic pain.

Project description:Brain structure and function are tightly correlated across all animals. While these relations are ultimately manifestations of differently wired neurons, many changes in neural circuit architecture lead to larger-scale alterations visible already at the level of brain regions. Locating such differences has served as a beacon for identifying brain areas that are strongly associated with the ecological needs of a species-thus guiding the way towards more detailed investigations of how brains underlie species-specific behaviors. Particularly in relation to sensory requirements, volume-differences in neural tissue between closely related species reflect evolutionary investments that correspond to sensory abilities. Likewise, memory-demands imposed by lifestyle have revealed similar adaptations in regions associated with learning. Whether this is also the case for species that differ in their navigational strategy is currently unknown. While the brain regions associated with navigational control in insects have been identified (central complex (CX), lateral complex (LX) and anterior optic tubercles (AOTU)), it remains unknown in what way evolutionary investments have been made to accommodate particularly demanding navigational strategies. We have thus generated average-shape atlases of navigation-related brain regions of a migratory and a non-migratory noctuid moth and used volumetric analysis to identify differences. We further compared the results to identical data from Monarch butterflies. Whereas we found differences in the size of the nodular unit of the AOTU, the LX and the protocerebral bridge (PB) between the two moths, these did not unambiguously reflect migratory behavior across all three species. We conclude that navigational strategy, at least in the case of long-distance migration in lepidopteran insects, is not easily deductible from overall neuropil anatomy. This suggests that the adaptations needed to ensure successful migratory behavior are found in the detailed wiring characteristics of the neural circuits underlying navigation-differences that are only accessible through detailed physiological and ultrastructural investigations. The presented results aid this task in two ways. First, the identified differences in neuropil volumes serve as promising initial targets for electrophysiology. Second, the new standard atlases provide an anatomical reference frame for embedding all functional data obtained from the brains of the Bogong and the Turnip moth.

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

Publications

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

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