Theses Doctoral

Food-caching birds as a model for systems neuroscience: behavioral, anatomical, and physiological foundations

Applegate, Marissa Claire

Food-caching birds like black-capped chickadees offer unique advantages for studying neural processes underlying episodic memory. Chickadees exhibit prodigious memories—they can cache thousands of food items throughout their environment and use memory to navigate back to these hidden food stores. Additionally, their hippocampal circuit is simplified relative to that of mammals, containing far fewer inputs and outputs. However, little work had been done to understand the neural processes underlying these animal’s memory abilities. This thesis details several projects that aimed to better establish food-caching birds as an animal model of memory for systems neuroscience.

In Chapter 2, we described the creation of behavioral tasks to utilize the chickadees’ natural memory behavior. Here, we monitored chickadees’ behavior while they cached food into a grid of sites covered by rubber flaps. We then applied probabilistic modeling to examine how different strategies guided birds’ choices during caching and retrieval. Chickadees used memories of the contents of individual cache sites in a context-dependent manner, avoiding sites that contained food during caching and returning to those same sites during retrieval. These results demonstrate memory flexibility in an animal in a tractable spatial paradigm.

In Chapter 3, we asked whether the bird brain had a region that was similar to the entorhinal cortex. We found that the dorsal lateral hippocampal formation (DL/CDL), one of the main inputs to the chickadee hippocampus, sharded marked anatomical and physiological similarities to the mammalian entorhinal cortex. We first used retrograde and anterograde tracing to examine the connectivity between DL/CDL and the hippocampus, as well as DL and the rest of the pallium. We found that the topographic patterns of DL/CDL input were similar to those of the mammalian entorhinal cortex. We next examined the physiology of DL, using 1-photon calcium imaging to monitor neural activity while birds performed a random foraging task. Like the entorhinal cortex, DL contained multi-field ‘grid-like’ spatial neurons, as well as border cells, head direction cells and speed-tuned cells. Collectively, these results establish DL/CDL as an entorhinal cortex analog.

In Chapter 4, we expanded the anatomical analysis to examine all of the inputs to the hippocampal formation. We varied our injections of retrograde tracers along the hippocampal long and transverse axes to examine if, like in mammals, there were topographic input patterns along these major axes. We found many patterns in input that were highly reminiscent of mammalian connectivity: like in rodents, visual pallial input preferentially innervated the septal portion of the hippocampus, while amygdala input preferentially targeted the temporal portion. These results further solidify the homology between the mammalian and avian hippocampal formations.

Collectively, through these sets of experiments, we have laid the groundwork for studying the black-capped chickadee in a modern neuroscience context.


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More About This Work

Academic Units
Neurobiology and Behavior
Thesis Advisors
Aronov, Dmitriy
Ph.D., Columbia University
Published Here
April 5, 2023