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Five Decades of Hippocampal Place Cells and EEG Rhythms in Behaving Rats

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Five Decades of Hippocampal Place Cells and EEG Rhythms in Behaving Rats 1 • The Journal of Neuroscience • 1–7 Viewpoints Five Decades of Hippocampal Place Cells and EEG Rhythms in Behaving Rats X Laura Lee Colgin Department of Neuroscience, Center for Learning and Memory, University of Texas at Austin, Austin, Texas 78712 Overthelast50years,muchhasbeenlearnedaboutthephysiologyandfunctionsofthehippocampusfromstudiesinfreelybehavingrats. Tworelativelyearlyworksinthefieldprovidedmajorinsightsthatremainrelevanttoday.Here,Irevisitthesestudiesanddiscusshowour understanding of the hippocampus has evolved over the last several decades. Introduction Although electrodes were placed in the medulla in the original report When I was given the opportunity to write this article describing (Ainsworth et al., 1969), it did not take long for O’Keefe and others to set how our understanding of hippocampal physiology and function their sights on the hippocampus. In a subsequent study, O’Keefe and Dostrovsky (1971) implanted electrodes in the hippocampus to record has changed since the time of the first annual Society for Neuro- how hippocampal spiking activity was affected by different behaviors science meeting, I thought a lot about how to approach the topic. (e.g., walking, orienting, sniffing, sleeping, etc.) and presentation of var- I was told to write this from my own perspective, while also ious sensory stimuli. In this initial short report, they described 8 putative focusing on interesting changes that have happened in the field neurons in the dorsal hippocampus that fired at particular locations in over the last several years. I decided to revisit works written the testing environment and hypothesized that a function of the hip- shortly after the time of the first Society for Neuroscience meeting pocampus is to create and store a map of space. Five years later, O’Keefe that greatly impacted the hippocampal field and had a major (1976) published a more thorough study reporting that place cells, neu- influence on my own work. I will also discuss examples of more rons in the hippocampus that fire when a rat moves through a particular recent studies that built upon these foundations to advance our location in the environment, are a major cell type in the hippocampus. understanding of hippocampal physiology and function. I focus This paper was shortly followed by the publication of a book that has on findings related to two of my favorite areas of hippocampal been called “a bible in the study of spatial coding in the hippocampal formation” (Moser et al., 2017), The hippocampus as a cognitive map research: place cells and EEG rhythms. The insights provided by (O’Keefe and Nadel, 1978). these decades-old works remain highly significant and relevant to The Introduction of this highly influential book states the work’s pur- our modern understanding of the hippocampus. pose: “We shall argue that the hippocampus is the core of a neural mem- ory system providing an objective spatial framework within which the Place cells and the enduring influence of The hippocampus as items and events of an organism’s experience are located and interre- a cognitive map (O’Keefe and Nadel, 1978) lated” (O’Keefe and Nadel, 1978). This viewpoint remains widely held What was known about the hippocampus in 1969, the year when the first today (Lisman et al., 2017), at least for many nonhuman species, and the Society for Neuroscience meeting was held? A decade earlier, Scoville and finding that place cells fire in specific spatial locations in a given environ- Milner (1957) had published their groundbreaking report that assessed ment has been replicated by numerous laboratories. human patients who had hippocampal damage after undergoing neuro- Our understanding of place cells has since expanded to include find- surgery to remove parts of their medial temporal lobes. The amnesia ings showing that hippocampal “complex-spike cells,” the term used at observed in these patients, including patient H.M., for events experi- the time to describe putative pyramidal cells, also represent many non- enced after their surgeries led researchers to conclude that the primary spatial aspects of experience. Initial influential studies from the late Bob function of the hippocampus is episodic memory. Before this work, other Muller, his long-time collaborator John Kubie, and other colleagues theories of hippocampal function had been put forward, including hy- showed that changing the stimuli associated with an environment (e.g., potheses that the hippocampus is involved in emotion, olfaction, and color, shape, light vs darkness) could change the firing patterns of place attention (Andersen et al., 2007). cells (Muller and Kubie, 1987; Quirk et al., 1990; Bostock et al., 1991). In In 1969, John O’Keefe and colleagues described an important techni- 1999, Emma Wood, Paul Dudchenko, and the late Howard Eichenbaum cal breakthrough that would allow future studies to directly relate activity published a groundbreaking study recording responses of complex spike of neurons to animals’ behavior and performance on behavioral tasks. cells in rats performing an olfactory memory task (Wood et al., 1999). They found that cells in hippocampal subregions CA3 and CA1 re- sponded selectively to salient, nonspatial aspects of the animal’s experi- Received April 1, 2019; revised Aug. 19, 2019; accepted Aug. 22, 2019. ence, including odor and trial condition (i.e., match or nonmatch). Since This work was supported by National Science Foundation Career Award 1453756, National Institutes of Health then, subsequent studies have shown that place cells represent tactile Award R01MH102450, and Department of Defense Congressionally Directed Medical Research Program Award (Gener et al., 2013), auditory (Aronov et al., 2017), and taste (Herzog et W81XWH1810314. The author thanks Ernie Hwaun for help with preparation of Figure 3. The authors declare no competing financial interests. al., 2019) information. Correspondence should be addressed to Laura Lee Colgin at [email protected]. Yet, place cells are not simply computing a conjunctive response to https://doi.org/10.1523/JNEUROSCI.0741-19.2019 multimodal sensory stimuli. Various lines of evidence indicate that place Copyright © 2019 the authors cell responses change according to animals’ past experiences. Place cells 2 • J. Neurosci. • 1–7 Colgin • Hippocampal Place Cells and EEG Rhythms were shown to change their firing patterns in specific environments in which fear condition- ing occurred (Moita et al., 2004). However, ex- periences do not have to be aversive to significantly change place cell activity. In an experiment by Jill Leutgeb and colleagues (2005), place cells in rats were recorded across successive sessions in an environment that was gradually morphed from a square to a circle, and vice versa, through a series of intermediate AAAB AB ABC ABC BCD BCD CD CDD D shapes. Place cell firing patterns in intermedi- ate shapes more closely resembled firing pat- Figure1. Sequencesofplacecellsfiringwithinindividualthetacyclesaredepictedinaschematic.Fourplacecellswithpartially terns in the square or circle when the square or overlapping place fields are depicted in a rat who is running to the right. Individual theta cycles are separated by black horizontal circle, respectively, was presented first in the lines. Note how organized place cells fire across successive theta cycles as the rat runs through their place fields. Theta sequences sequence (Leutgeb et al., 2005). Moreover, in a are apparent in the middle theta cycles, with place cells having place fields at earlier and later locations firing at earlier and later follow-up study, place cell firing patterns were theta phases, respectively. Reproduced with permission from Skaggs et al. (1996). found to gradually change across intermediate morph shapes in rats that had been pretrained view. In hippocampal subregion CA2, place cells’ firing patterns change in a constant location. In contrast, in rats that had been previously over the time course of hours in constant spatial environments (Mankin trained in square and circle environments placed in separate locations, et al., 2015). Another study measuring large numbers of CA1 place cells place cell firing patterns in square-like intermediate shapes remained simultaneously in freely behaving mice reported that the specific ensem- similar to those in the square and abruptly changed to resemble firing ble of place cells representing a particular environment changed across patterns in the circle when animals were placed in circle-like intermedi- days when environmental conditions were held constant (Ziv et al., ate environments (Colgin et al., 2010). Place cells’ firing rates also change 2013). From day to day, a mixed pattern was observed, with some cells according to where an animal was in the recent past or where an animal maintaining relatively stable firing patterns from one day to the next and is heading in the future (Frank et al., 2000; Wood et al., 2000; Ferbinteanu others changing their firing patterns. However, another recent study and Shapiro, 2003). Moreover, place cell firing becomes more anticipa- involving calcium imaging of place cells in freely behaving mice sug- tory with experience. That is, place cells start firing earlier and earlier gested that much of the instability observed in earlier studies may reflect before the center of their place fields as animals gain experience in an a coherent reorientation of place cell maps to a different environmental environment (Mehta et al., 1997, 2000; Ekstrom et al., 2001;
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