Sensory- and Motor-Related Responses of Layer 1 Neurons in the Mouse Visual Cortex

J Neurosci. 2019 Dec 11;39(50):10060-10070. doi: 10.1523/JNEUROSCI.1722-19.2019. Epub 2019 Nov 4.

Abstract

Cortical layer 1 (L1) contains a sparse and molecularly distinct population of inhibitory interneurons. Their location makes them ideally suited for affecting computations involving long-range corticocortical and subcortical inputs, yet their response properties remain largely unexplored. Here we attempt to characterize some of the functional properties of these neurons in the primary visual cortex of awake mice. We find that the strongest driver of L1 neuron activity is locomotion, with at least half of L1 neurons displaying locomotion-related activity. Visual responses are present in a similar fraction of neurons, but these responses are weaker and frequently suppressive. We also find that ∼43% of L1 neurons respond to noise stimuli and at least 14% respond to whisker touch, with these two populations being statistically independent. Finally, we find that 45% of L1 neurons have generally weak responses correlated with whisking activity. Overall, the spatial distributions of modality-specific responses were more or less random. Our work helps to establish the basic sensory- and motor-related responses of L1 interneurons, revealing several previously unreported characteristics.SIGNIFICANCE STATEMENT Cortical processing even in primary sensory areas is strongly influenced by nonlocal corticocortical and neuromodulatory inputs. Many of these inputs are known to converge onto layer 1 where they target not only distal dendrites of pyramidal neurons but also a sparse population of inhibitory neurons. Previous studies have suggested that layer 1 neurons may play a crucial role in mediating the effects of these long-range projections, but the different types of inputs have mostly been studied in isolation. Here, we take a closer look at the response properties of layer 1 neurons in mouse visual cortex, examining both their visual properties, likely caused by direct thalamocortical inputs, and other sensory and motor properties, likely reflecting corticocortical and neuromodulatory inputs.

Keywords: Ca2+ imaging; awake mouse; functional response properties; inhibitory neuron; multimodal; visual cortex.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Calcium / metabolism
  • Female
  • Interneurons / physiology
  • Locomotion / physiology*
  • Male
  • Mice
  • Neural Pathways / physiology
  • Neurons / physiology*
  • Patch-Clamp Techniques
  • Physical Stimulation
  • Touch / physiology
  • Vibrissae
  • Visual Cortex / physiology*

Substances

  • Calcium