The chickadee as a model for neuroscience
Food caching is used by many animals to cope with instabilities in their food supply. A small number of bird families, including Corvidae (e.g. crows and jays) and Paridae (e.g. chickadees and titmice) employ a unique strategy of scattering hidden caches throughout an environment and using episodic memory to find these caches later in time. The capacity of this behavior is astonishing: in extreme climates, chickadees have been observed making 5,000 caches per day. They can precisely remember their caches using the hippocampus — a structure critically involved in memory across all vertebrates, including humans. The hippocampus of food-caching species is three times larger than that of non-caching species and even changes in size seasonally.
An appealing feature of food caching is that memory storage in this behavior occurs at numerous discrete, well-defined points in time. These moments are perfect for analyzing or manipulating neural activity. Our lab has pioneered experimental paradigms for the black-capped chickadee (Poecile atricapillus) — a common North American songbird that adapts particularly well to laboratory conditions. Chickadee behavior and neuroanatomy are exciting new targets for the tools of 21st-century neuroscience.
Black-capped chickadee attempting to cache a piece of acorn pulp in a crevice between branches.
Central Park, New York City. Photo by D. Aronov.
Distribution of some caches made in a forest by a marsh tit, a species closely related to chickadees.
Based on: Shettleworth 1983
Food caching in the lab
Chickadees are an arboreal species and have been studied mostly in large, naturalistic environments. It is a major challenge to bring their food-caching behavior into laboratory settings compatible with the tools of modern neuroscience. Our lab has developed behavioral arenas that contain many concealed sites for caching, but are compatible with neural recordings and detailed behavioral tracking. A chickadee in our arena lifts a cover flap to access a cache site, providing an unambiguous readout of its behavior. Cameras track movements of the bird and even the contents of all the cache sites. We have developed computer vision algorithms for postural tracking of a tiny animal in a large physical space, and have used real-time video analysis for closed-loop manipulations. In spite of being in a compact lab setting, chickadees in our arenas use memory, both to choose sites for caching and to retrieve food later in time. As in the wild, these memories are long-lasting and spatially precise.
Chickadee caching seeds in a laboratory area.
Initial description: Applegate and Aronov 2022
Video from: Chettih et.al. 2023
Six camera views of chickadee behavior. Neural networks crop all views and perform 3D postural reconstruction.
From: Chettih et.al. 2023
Neural circuits for food cache memory
The hippocampus is a neural circuit critical for forming memories in all vertebrates, including humans. A challenge of studying this circuit is its enormous complexity. In mammals, the hippocampal formation (which also includes the entorhinal cortex) consists of at least nine distinct regions, connected to nearly 30 cortical areas and similarly numerous subcortical structures. The avian brain offers a solution to this problem. Birds have a hippocampal formation derived from the same embryological precursor as its mammalian counterpart (the medial pallium). Our lab has shown that this structure even includes an entorhinal-like region. However, the avian hippocampal formation is connected to a much smaller number of inputs and outputs. We have mapped these regions in chickadees. As in other parts of the avian brain, both cortical and subcortical areas of the hippocampal circuit are organized into well-defined, well-separated clusters of cells (nuclei). A small number of easily targetable nuclei makes the bird hippocampal formation an ideal circuit for neural recordings and manipulations.
The avian hippocampal formation is rotated by roughly 90° relative to rodents and is on the brain surface. Colors: topographic organization of entorhinal-like regions.
From: Applegate et.al. 2023a
Chickadee brain. Dark gray: the left hippocampus. Colors: the four cortical (pallial) inputs into the left hippocampal formation, excluding the entorhinal-like DL/CDL.
Based on: Applegate et.al. 2023b
Neural recordings in chickadees
Chickadees are tiny — about 11 grams, or less than half the weight of a laboratory mouse. Food caching requires them to move over a relatively large space, making vigorous and dexterous movements with their heads. These are major challenges for neural recordings. Our lab has engineered miniaturized technologies for dense neural recordings in these challenging conditions. We routinely use silicon probes and have developed “semi-acute” protocols that allow recording stable numbers of units for multiple weeks of an experiment. We have also adapted head-mounted microscopy for chickadees, taking advantage of the fact that the avian hippocampal formation is at the dorsal brain surface.
Our discoveries include place cells in birds — the first time that these spatial firing patterns have been demonstrated in the brain on any non-mammal. Other findings include hippocampal sharp-wave ripples, as well as diverse entorhinal-like patterns, including grid-like cells, in DL/CDL (a region anatomically analogous to the entorhinal cortex). These findings demonstrate a remarkable similarity of hippocampal function across 320 million years of evolution. Following these foundational results, we have begun to unravel how episodic memories are represented in the brain.
Spatial maps of 160 simultaneously recorded hippocampal neurons in the chickadee, sorted by spatial information (horizontally), then by firing rate. Many cells are place cells. High-firing, weakly spatial cells are putative interneurons.
Initial findings: Payne et.al. 2021
Data from: Chettih et.al. 2023
Silicon probe recording in the chickadee hippocampus. Left and right plots are two shanks of the probe. Channels are sorted from superficial to deep. Recording shows sharp-wave ripples (SWRs) — synchronous events across electrodes.
Initial findings: Payne et.al. 2021
Data from: Chettih et.al. 2023