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Brain Rhythms and Short-Term Memory Earl K. Miller

Brain Rhythms and Short-Term Memory Earl K. Miller The Picower Institute for Learning and Memory and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology www.ekmiller.org Adler Foundation Symposium February 2010. Our Goal:

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Brain Rhythms and Short-Term Memory Earl K. Miller

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  1. Brain Rhythms and Short-Term Memory Earl K. Miller The Picower Institute for Learning and Memory and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology www.ekmiller.org Adler Foundation Symposium February 2010

  2. Our Goal: To understand the neural basis of high-level cognition. Human The prefrontal cortex Monkey • Our Approach: • Multiple-electrode recording in trained monkeys. • Allows detailed comparisons of the timing of activity between neurons.

  3. How Do We Hold Multiple Thoughts in Mind? The ability to hold multiple items in short-term memory is critical for planning and executing goal-directed behavior. Increasing evidence for a role of oscillatory activity in short-term memory. One model suggests phase-dependent coding of memory items (e.g., Lisman and Idiart, Science, 1995). This model attempted to explain why short-term memory has a severe limitation in capacity.

  4. Cognitive capacity: How many things can you hold in mind simultaneously? Capacity is highest in younger adults and reduced in many neuropsychiatric disorders Schizophrenia Parkinson’s Disease It is linked to normal cognition and intelligence: Individual differences in capacity limits can explain about 25-50% of the individual differences in tests of intelligence www.ekmiller.org Vogel et al (2001); Gold et al (2003); Cowan et al (2006); Hackley et al (2009)

  5. How Does the Brain Hold Multiple Items in Memory? Q1: Is there oscillatory synchronization during short-term memory? Q2: Do spikes at particular phases of LFP oscillations carry more information about items in memory? Q3: Is there more information about different memory items in different LFP phases?

  6. Behavioral Task and Neurophysiological Recording • Two monkeys • New stimulus set (4 objects) each day. Object identity fully balanced with order. • Eight electrodes simultaneously implanted in the DL prefrontal cortex • Local field potentials and multi-unit spikes from 140 recording sites Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  7. Sustained LFP Gamma Oscillations During Memory Delays Average of all randomly selected spikes 2nd delay(two stimuli sequence) 1st delay(one stimulus) LFP power at differentfrequencies Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  8. Q1: Is thereoscillatory synchronization during short-term memory? Yes Average of all randomly selected spikes 2nd delay(two stimuli sequence) 1st delay(one stimulus) LFP power at differentfrequencies Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  9. Do Spikes Synchronize to LFP Oscillations? Preferred spiking phase across recording sites 32 Hz Proportion of recording sites with significant spike-LFP phase-locking 3 Hz Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  10. Q2: Do spikes at particular phases of LFP oscillations carry more information about items in memory? Yes Preferred spiking phase across recording sites 32 Hz Proportion of recording sites with significant spike-LFP phase-locking 3 Hz Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  11. Stimulus Information in Average Spiking Activity Average firing rate does not clearly distinguish object order Information about stimulus identity (Neural variance explained by stimulus factor) Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  12. Stimulus Information in Average Spiking Activity By LFP Phase Information about stimulus identity from spiking activity in each LFP phase bin. Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  13. Stimulus Information By Stimulus Order in Different LFP Phases 32 Hz LFP Power Stimuli were balanced by order Objects were balanced by order Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  14. Object Information By Object Order in Different LFP Phases 32 Hz Coding of objects in different phases was observed at 32 Hz, not 3 Hz 3 Hz Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  15. Object Information By Object Order in Different LFP Phases 32 Hz Even though overall spike-phase synchrony is unchanged Error trials (32 Hz) (corrects + errors) Object phases overlap Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  16. Q3: Is there more information about different memory items in different LFP phases? Yes 32 Hz Even though overall spike-phase synchrony is unchanged Error trials (32 Hz) (corrects + errors) Object phases overlap Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  17. Conclusions During short-term memory, prefrontal activity shows oscillatory synchronization in gamma and theta bands. Spikes carry more information about stimuli held in memory at particular LFP phases. The first stimulus of the memorized sequence is encoded earlier in the LFP cycle than the second stimulus for the gamma band but not the theta band. Phase-dependent coding may serve to flexibly represent sequences in memory on a generic neuronal time-scale. Gamma band = spike-timing dependent plasticity? This may also explain why short-term memory has a capacity limitation. Siegel, Warden, and Miller (2009) Proc. Nat. Acad. Sci.

  18. Miller Lab Oct 2009 www.ekmiller.org

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