Revealing neocortical mechanisms for declarative learning: Functional role and cellular mechanisms of primary sensory cortex plasticity for trace eyeblink conditioning in mice.
Final Report Abstract
Associative learning is characterized by sensible alterations in the behavior of a subject in response to relevant changes in the world. In case the sensory stimulus signaling the changed environment is temporally separate from the to-be-adapted behavior, the association of the two requires mnemonic brain processes. In trace eyeblink conditioning (TEBC) the temporal gap between the conditioned (CS) and the unconditioned stimulus is bridged by sustained neuronal activity in prefrontal cortex. We studied the role of primary somatosensory cortex (S1) for TEBC. We trained mice on a tactile variant of TEBC, taking advantage of the very well-studied whiskerrelated part of S1, the so-called barrel cortex. We found that S1 undergoes a strong synaptic rearrangement during TEBC, and prominently holds learning-related and mnemonic signals. Dendritic spines on apical dendrites of L5 pyramids in L1 were found to be eliminated to a large part during trace conditioning. Using multi-site electrophysiology in head-fixed behaving mice trained on TEBC, we found significant differences of field potentials and action potential rates during the periods of steepest advance of learning. These plastic changes were localized throughout cortical layers with a focus on infragranular layers. Changes were observed during the later epoch of CS presentation, but interestingly also during the mnemonic Trace period. Causal interference in S1 activity using optogenetic blockade of S1 indicated that neuronal activity during the CS affects acquisition of learning, but not its retention, while learning related and mnemonic activity during Trace was not needed for learning. These results revealed complex features of S1 participation in mnemonic processes when the animal is engaged in tactile learning tasks. One speculation is that S1 contributes to explicit (in humans sometimes called ‘declarative’) learning systems that associate the conditioned stimulus to movement for purposes of rule learning, i.e. executive functions. Explicit learning would no normally be read out by the TEBC paradigm, which solely reports the learning of a movement (the conditioned response), typically considered a type of implicit learning. Further, our results open interesting questions about the dynamic role of learning related neuronal activity in S1 and in fact across the large parts of the neocortex including prefrontal areas. Future work will need to elucidate the role of S1 and its learning related activities for consolidation of the learned behavior.
Publications
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(2015) Corticofugal projection patterns of whisker sensorimotor cortex to the sensory trigeminal nuclei. Front. Neural Circuits 9:53
Smith, J.B., Watson, G.D., Alloway, K., Schwarz, C.,Chakrabarti S.
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(2015) Spine loss in primary somatosensory cortex during trace eyeblink conditioning. J Neurosci, 35:3772-3781
Joachimsthaler, B., Brugger, D., Skodras, A., Schwarz, C.
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(2015) Support for the slip hypothesis from whisker-related tactile perception of rats in a noisy environment. Front Integr Neurosci. 9:53
Waiblinger, C., Brugger, D., Whitmire, C.J., Stanley, G.B., Schwarz C.
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(2015) Vibrotactile discrimination in the rat whisker system is based on neuronal coding of instantaneous kinematic cues. Cereb Cortex 25:1093–1106
Waiblinger, C., Brugger, D., Schwarz C.
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(2015) Whisking control by motor cortex., Scholarpedia, 10(3):7466
Schwarz, C., Chakrabarti, S.
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(2016) Information coding through adaptive gating of synchronized thalamic bursting. Cell Rep 14:795–807
Whitmire, C.J., Waiblinger, C., Schwarz C., Stanley, G.B.
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(2016) The slip hypothesis: Tactile perception and its neuronal bases. Trends Neurosci 39:449–4
Schwarz C.
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(2018) Barrel cortex: What is it good for? Neuroscience 368: 3–16
Stüttgen, M.C., Schwarz, C.
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(2018) Biomechanical texture coding in rat whiskers. Sci. Rep. 8:11139
Oladazimi, M., Brendel, W., Schwarz, C
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(2018) Cortical modulation of sensory flow during active touch in the rat whisker system. Nat. Commun. 9:3907
Chakrabarti, S., Schwarz, C.
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(2018) Global coding in rat barrel cortex in the absence of local cues. Cereb Cortex, 28:2015-2027
Gerdjikov, T.V., Bergner, C.G., Schwarz, C.
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(2018) Lifting the veil on the dynamics of neuronal activities evoked by transcranial magnetic stimulation. eLife pii: e30552
Li B., Virtanen J.P., Oeltermann A., Schwarz C., Giese M.A., Ziemann U., Benali A.
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(2018) Primary tactile thalamus spiking reflects cognitive signals. J. Neurosci. 38:4870-4885
Waiblinger, C. Whitmire, C.J., Sederberg, A., Stanley, G.B., Schwarz, C.
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(2019) Effects of diazepam on low-frequency and highfrequency electrocortical γ-power mediated by α1- and α2-GABAA receptors. Int.J.Mol.Sci. 20:3486
Hofmann, J.I., Schwarz, C., Rudolph, U., Antkowiak, B.
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(2020) A tactile virtual reality for the study of active somatosensation. Front Integr Neurosci 14:1–15
Bhattacharjee A., Kajal D.S., Patrono A., Hegner Y.L., Zampini M., Schwarz C., Braun C.
