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J Neurosci. 2015 Sep 9;35(36):12560-73. doi: 10.1523/JNEUROSCI.2240-15.2015.

Specific Early and Late Oddball-Evoked Responses in Excitatory and Inhibitory Neurons of Mouse Auditory Cortex.

Author information

  • 1Laboratory of Neural Circuit Dynamics, Brain Research Institute, University of Zurich, CH-8057, Zurich, Switzerland, Neuroscience Center Zurich, University of Zurich and ETH Zurich, CH-8057, Zurich, Switzerland, and.
  • 2Laboratory of Neural Circuit Dynamics, Brain Research Institute, University of Zurich, CH-8057, Zurich, Switzerland, Neuroscience Center Zurich, University of Zurich and ETH Zurich, CH-8057, Zurich, Switzerland, and hluetcke@ethz.ch helmchen@hifo.uzh.ch.
  • 3Laboratory of Neural Circuit Dynamics, Brain Research Institute, University of Zurich, CH-8057, Zurich, Switzerland, Scientific IT Services, ETH Zurich, CH-8092, Zurich, Switzerland hluetcke@ethz.ch helmchen@hifo.uzh.ch.

Abstract

A major challenge for sensory processing in the brain is considering stimulus context, such as stimulus probability, which may be relevant for survival. Excitatory neurons in auditory cortex, for example, adapt to repetitive tones in a stimulus-specific manner without fully generalizing to a low-probability deviant tone ("oddball") that breaks the preceding regularity. Whether such stimulus-specific adaptation (SSA) also prevails in inhibitory neurons and how it might relate to deviance detection remains elusive. We obtained whole-cell recordings from excitatory neurons and somatostatin- and parvalbumin-positive GABAergic interneurons in layer 2/3 of mouse auditory cortex and measured tone-evoked membrane potential responses. All cell types displayed SSA of fast ("early") subthreshold and suprathreshold responses with oddball tones of a deviant frequency eliciting enlarged responses compared with adapted standards. SSA was especially strong when oddball frequency matched neuronal preference. In addition, we identified a slower "late" response component (200-400 ms after tone onset), most clearly in excitatory and parvalbumin-positive neurons, which also displayed SSA. For excitatory neurons, this late component reflected genuine deviance detection. Moreover, intracellular blockade of NMDA receptors reduced early and late responses in excitatory but not parvalbumin-positive neurons. The late component in excitatory neurons thus shares time course, deviance detection, and pharmacological features with the deviant-evoked event-related potential known as mismatch negativity (MMN) and provides a potential link between neuronal SSA and MMN. In summary, our results suggest a two-phase cortical activation upon oddball stimulation, with oddball tones first reactivating the adapted auditory cortex circuitry and subsequently triggering delayed reverberating network activity. Significance statement: Understanding how the brain encodes sensory context in addition to stimulus feature has been a main focus in neuroscience. Using in vivo targeted whole-cell recordings from excitatory and inhibitory neurons of mouse primary auditory cortex, we report two temporally distinct components of membrane potential responses encoding oddball tones that break stimulus regularity. Both components display stimulus-specific adaptation upon oddball paradigm stimulation in the three recorded cell types. The late response component, in particular, carries signatures of genuine deviance detection. In excitatory but not parvalbumin-positive inhibitory neurons, both early and late components depend on NMDA receptor-signaling. Our work proposes a potential neuronal substrate of a known deviant-evoked event-related potential, which is of fundamental significance in basic and clinical neuroscience.

KEYWORDS:

auditory cortex; interneurons; mismatch negativity; mouse; stimulus-specific adaptation

PMID:
26354921
DOI:
10.1523/JNEUROSCI.2240-15.2015
[PubMed - indexed for MEDLINE]
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