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Memory trace and timing mechanism localized to cerebellar Purkinje cells

  1. Germund Hesslowa,b
  1. aAssociative Learning Group, Department of Experimental Medical Science, Lund University, S-221 84 Lund, Sweden;
  2. bThe Linnaeus Center Thinking in Time: Cognition, Communication and Learning, Lund University, S-222 00 Lund, Sweden; and
  3. cLaboratory for Synthetic Perceptive, Emotive, and Cognitive Systems, Department of Information and Communications Technologies, Universitat Pompeu Fabra, 08018 Barcelona, Spain

  1. Edited* by Charles R. Gallistel, Rutgers University, Piscataway, NJ, and approved September 8, 2014 (received for review August 9, 2014)

Significance

The standard view of neural signaling is that a neuron can influence its target cell by exciting or inhibiting it. An important aspect of the standard view is that learning consists of changing the efficacy of synapses, either strengthening (long-term potentiation) or weakening (long-term depression) them. In studying how cerebellar Purkinje cells change their responsiveness to a stimulus during learning of conditioned responses, we have found that these cells can learn the temporal relationship between two paired stimuli. The cells learn to respond at a particular time that reflects the time between the stimuli. This finding radically changes current views of both neural signaling and learning.

Abstract

The standard view of the mechanisms underlying learning is that they involve strengthening or weakening synaptic connections. Learned response timing is thought to combine such plasticity with temporally patterned inputs to the neuron. We show here that a cerebellar Purkinje cell in a ferret can learn to respond to a specific input with a temporal pattern of activity consisting of temporally specific increases and decreases in firing over hundreds of milliseconds without a temporally patterned input. Training Purkinje cells with direct stimulation of immediate afferents, the parallel fibers, and pharmacological blocking of interneurons shows that the timing mechanism is intrinsic to the cell itself. Purkinje cells can learn to respond not only with increased or decreased firing but also with an adaptively timed activity pattern.

Footnotes

  • ↵1To whom correspondence should be addressed. Email: fredrik.johansson{at}med.lu.se.

  • Author contributions: F.J., D.-A.J., and G.H. designed research; F.J. and R.Z. performed research; F.J. and A.R. analyzed data; and F.J. and G.H. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a Prearranged Editor.

Freely available online through the PNAS open access option.

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