Electrophysiological signatures of learning in the hippocampus
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1
University of Jyväskylä, Department of Psychology, Finland
BACKGROUND: Hippocampal electrophysiological activity in awake rats and rabbits is characterized by alternating epochs of rhythmic activity at the theta band (3-12 Hz) and the occurrence of sharp wave-ripple complexes (SPW-Rs, 100-250 Hz). Theta is most commonly present during voluntary movement (running) and in anticipation of external events such as when the smell of a predator is present. In contrast, SPW-Rs mostly take place during immobility. Both theta and ripples are linked to learning and memory: According to the so-called two-stage model (Buzsáki, 1989), theta is indicative of a state in which information arriving from the neocortex is encoded into hippocampal neuronal networks by granule cells. SPW-Rs, on the other hand, are initiated during the following rest periods in the hippocampal CA3 and result in synchronous firing of thousands of pyramidal cells in the CA1. It is thought that SPW-Rs result in information transfer from the hippocampus back to the neocortex for long-term memory storage.
GOALS: For several years our group has been focused on finding out how spontaneously occurring theta and ripples affect associative learning.
METHODS: We use classical eyeblink conditioning as a model of associative learning. In this task, a warning signal (conditioned stimulus) is presented first, followed by an unpleasant stimulation of the eyelid (unconditioned stimulus). The unconditioned stimulus always elicits an eyeblink, the unconditioned response. As a result of repeated presentations of the conditioned stimulus paired with the unconditioned stimulus, the conditioned stimulus alone starts to elicit an eyeblink. This is called the conditioned response. During eyeblink conditioning in rats and rabbits we record hippocampal electrophysiological activity, namely the extracellular local-field potential (LFP) reflecting the summed synaptic currents of thousands of cells in the vicinity of the recording electrode. From the LFP we then detect certain events on-line, for example the occurrence of SPW-Rs, and further use this information to align the presentation of the external stimuli, for example the conditioned stimulus.
A 10-second example of LFP recorded from the CA1 pyramidal layer of the hippocampus in an awake, restrained rabbit is shown in Figure 1.
RESULTS: Our work so far indicates that both theta and SPW-Rs can be used to regulate learning rate: the state in which SPW-Rs take place appears to support associative learning as well as hinder extinction (Nokia et al., 2010). In contrast, the state in which theta is prominent seems to promote extinction (Nokia & Wikgren, 2014). Further, ongoing hippocampal theta seems to disrupt associative learning if the conditioned stimulus is timed to start at a certain phase of the oscillation (Nokia et al., 2015).
CONCLUSION: Based on our work so far, it is clear that there are many possibilities for neural markers to be used in the regulation of associative learning and extinction. Theta and SPW-Rs are easily detected by the naked eye from the LFP but other, more complex measures, such as coherence of electrophysiological activity in brain regions of choice could just as well be used. A future challenge will be to find ways to extend our results to use in humans.
Acknowledgements
This work was supported by the Academy of Finland, grant number 275954.
References
Buzsáki G. (1989). Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience, 31, 551-570.
Nokia, M.S., Penttonen, M., and Wikgren, J. (2010). Hippocampal ripple-contingent training accelerates trace eyeblink conditioning and retards extinction in rabbits. J Neurosci, 30, 11486-11492.
Nokia, M.S., Waselius, T., Mikkonen, J.E., Wikgren, J., and Penttonen, M. (2015). Phase matters: responding to and learning about peripheral stimuli depends on hippocampal θ phase at stimulus onset. Learn Mem, 22, 307-317.
Nokia, M.S., and Wikgren, J. (2014). Effects of hippocampal state-contingent trial presentation on hippocampus-dependent nonspatial classical conditioning and extinction. J Neurosci, 34, 6003-6010.
Keywords:
Hippocampus,
Eyeblink Classical Conditioning,
theta oscillations,
ripples,
SPW-R
Conference:
International Conference - Educational Neuroscience, Abu Dhabi, United Arab Emirates, 28 Feb - 29 Feb, 2016.
Presentation Type:
Oral Presentation (invited speakers only)
Topic:
Educational Neuroscience
Citation:
Nokia
MS
(2016). Electrophysiological signatures of learning in the hippocampus.
Front. Neurosci.
Conference Abstract:
International Conference - Educational Neuroscience.
doi: 10.3389/conf.fnins.2016.92.00021
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Received:
13 Jan 2016;
Published Online:
23 Mar 2016.
*
Correspondence:
Dr. Miriam S Nokia, University of Jyväskylä, Department of Psychology, Jyväskylä, Finland, miriam.nokia@jyu.fi