Rapid dynamics of hippocampal spatial representation in echolocating bats

bats-in-the-sky

For a recent neuroscience journal club, I presented several papers on echolocating bats. Under the premise that “bats are awesome” (F. Collman, personal communication), what follows are the major points from my presentation. The slideshow below contains parts of my presentation including figures from several relevant papers. A disclaimer – I will be vastly oversimplifying the research, and presenting only a fraction of what the authors discovered and discussed. For less concise descriptions of the research in question, interested persons should read the appropriate papers. The hippocampus is a region of the brain critically important for episodic and spatial memory. Patients without their hippocampi (like the famous patient H.M.) cannot form new episodic memories. Patient case studies such as H.M’s sparked a keen interest in the hippocampus amongst neuroscientists, and there have been great strides in elucidating the neural circuitry within the hippocampus. The question of exactly how that neural circuitry encodes episodic and spatial memory is a matter for many lines of ongoing research and much debate.

One well described phenomenon within the hippocampus, that may play a critical role in the spatial component of spatial memory formation, are hippocampal neurons termed “place cells”. These neurons are driven when the animal passes through a particular region of its environment. Earlier work in rodents demonstrated that when an animal is placed within a particular environment, its place cells tile the entire area, tracking the animal’s movements. The spatial region that any given place cell (called the “place field”) encodes is flexible – changes to the environment (i.e. moving landmarks, changing wall colors, altering odors) will alter the place field. Introducing an animal into a brand new environment will cause an individual place cell to generate a new place field, however returning that animal to the old environment will recall the original place field. Theoretically, the location information provided by place cells could be utilized in the generation of memories. Place cells fire as you move through the world, and the order in which the population fires could be stored as a memory of movement through space. Exactly how this storage could be achieved, and where in the brain it takes place, is the subject of many ongoing research projects. It’s also not what the rest of this post will be about.

Instead, we’ll turn to a slightly different question – one of how sensory information influences the structure of the place fields. Another persistent research question is what exact inputs generate the place field. It seems like common sense that sensory information would play some role in establishing and maintaining the place field, and in causing a place cell to fire as the animal moved through the appropriate place field. As I mentioned about, it is known that altering the sensory information within the environment will cause place cells to change their fields. However, these changes occurred over long time scales (the order of minutes to days). Researchers from the University of Maryland were interested in much quicker changes in place fields – namely, how place cells responded to newly arrived sensory information. Do place cells rapidly alter their fields based on temporally precise sensory events?

To answer this question, the researchers, Nachum Ulanovsky and Cynthia Moss turned to the big brown bat (Eptesicus fuscus). These echolocating bats, sized approximately 10 cm, produce echolocation calls on average once every 260 ms, which the bats preferentially use to provide sensory information about their environment. These calls, the authors reasoned, were the perfect sensory event with which they could investigate the possibility that the spatial precision of a place field is rapidly altered by sensory information. As a first step, the authors conclusively demonstrated place cells within the bat hippocampus; recording place fields while bats crawled along an angled wall, using echolocation to hunt for food (Ulanovsky and Moss, 2007). They then looked closely at the activity of place cells immediately after each echolocation call, and discovered that as time passed following a call, place fields got bigger (see Ulanovsky and Moss, 2011). In other words, after an echolocation call, place cell was pickier about the precise spatial region through which a bat had to move in order for that place cell to fire. This enhanced spatial precision lasted for ~ 300 ms after each call, demonstrating for the first time, rapid changes in hippocampal place fields tied to the influx of sensory information. The time constants of these changes (~300 ms) are much more rapid than those previously reported, which were on the order of seconds.

[slideshare id=11261716&doc=echolocationblogpresentation-120125174833-phpapp01]

Take home message:

Place cells can rapidly integrate incoming sensory information, tuning the spatial selectivity of their place cells to match the spatial acuity of the new information. The spatial selectivity decays between sonar calls as the animal has to rely on less accurate sensory information (or even do without any sensory information, depending on the availability of and preference for non-echolocation based sensory information).

What does this mean for non-bats? The research does make some interesting predictions for rodent or primate studies – namely that quickly providing visual information (perhaps by rapidly flashing on a strobe light) would lead to similar rapid place cell dynamics. However, whether the varying acuity of sensory information provides ongoing regulation of place fields in a more physiological context, is unclear. For example, animals with fovea (such as humans and non-human primates) can increase the acuity of visual information for a particular region of space by directing their fovea towards that region. Similarly, the process of attention is characterized by enhancements in the neural representations of sensory information. How these might influence the spatial selectivity of place fields remains an open question, as does the effect of rapid place field dynamics on the creation of spatial and episodic memory.

Ulanovsky and Moss (2007). Hippocampal cellular and network activity in freely moving echolocating bats. Nat. Neurosci 10(2): 224-233.

Ulanovsky and Moss (2011). Dynamics of hippocampal spatial representation in echolocating bats. Hippocampus 21:150-161.

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Astra Bryant

Astra Bryant is a graduate of the Stanford Neuroscience PhD program in the labs of Drs. Eric Knudsen and John Huguenard. She used in vitro slice electrophysiology to study the cellular and synaptic mechanisms linking cholinergic signaling and gamma oscillations – two processes critical for the control of gaze and attention, which are disrupted in many psychiatric disorders. She is a senior editor and the webmaster of the NeuWrite West Neuroblog