The excitatory neuronal microcircuit of the C2 column in the mouse primary somatosensory cortex

Rodents are nocturnal animals gathering information about their surroundings by using highly sensitive detectors laid out on their snout. Like humans use their fingertips to apprehend textures, rodents use their whiskers to build a spatial representation of their environment, locate objects and discriminate fine textures. The most remarkable feature of the somatosensory whisker system consists in the isomorphic correspondence of each whisker with discrete cytoarchitectonic units in layer 4 of the primary somatosensory "barrel" cortex. These layer 4 barrels are the first step towards the integration of the sensory information within the neocortex and form the core of each cortical barrel column. To further our understanding of sensory processing, it becomes evident that studying the synaptic wiring of a specific barrel column will provide useful information. In this thesis work, we specifically investigate the excitatory wiring diagram of the C2 barrel related column. The functional location of our preferred column was mapped in vivo using intrinsic optical imaging upon C2 whisker deflection. The excitatory microcircuit of the C2 barrel column was investigated in vitro using simultaneous multiple whole-cell patch clamp recordings in the current clamp mode. We show that layer 4, through its highly recurrent and strong network, acts as the main excitatory driving force, spreading information across the entire cortical column. We demonstrate that supragranular layers are involved both in intralaminar recurrent circuits and top-down relations with postsynaptic partners in specific subjacent layers. The last relay of the excitation flow consists of the infragranular layers that integrate input from the whole column, and form the output of the cortical computation. Finally, by assessing the diversity of short-term dynamics of a subset of excitatory connections, we point out the complexity of sensory processing and the long journey remaining to unravel the synaptic mechanisms underlying sensory perception.

Synaptic Computation and Sensory Processing in Neocortical Layer 2/3

Sylvain Crochet, Carl Petersen

Computations in neocortical circuits are predominantly driven by synaptic integration of excitatory glutamatergic and inhibitory GABAergic inputs. New optical, electrophysiological, and genetic methods allow detailed in vivo investigation of the superficial neocortical layers 2 and 3 (L2/3). Here, we review current knowledge of mouse L2/3 sensory cortex, focusing on somatosensory barrel cortex with comparisons to visual and auditory cortex. Broadly tuned, dense subthreshold synaptic input accompanied by sparse action potential (AP) firing in excitatory neurons provides a simple and reliable neural code useful for associative learning. Sparse AP firing is enforced by strong inhibition from genetically defined classes of GABAergic neurons. Subnetworks of strongly and specifically connected excitatory neurons may drive L2/3 network function, with potential contributions from dendritic spikes evoked by spatiotemporally clustered synaptic input. These functional properties of L2/3 are under profound regulation by brain state and behavior, providing interesting avenues for future mechanistic investigations into context-specific processing of sensory information.

Cell Press2013

Parallel pathways from whisker and visual sensory cortices to distinct frontal regions of mouse neocortex

Alexandros Kyriakatos, Céline Matéo, Carl Petersen, Varun Sreenivasan

The spatial organization of mouse frontal cortex is poorly understood. Here, we used voltage-sensitive dye to image electrical activity in the dorsal cortex of awake head-restrained mice. Whisker-deflection evoked the earliest sensory response in a localized region of primary somatosensory cortex and visual stimulation evoked the earliest responses in a localized region of primary visual cortex. Over the next milliseconds, the initial sensory response spread within the respective primary sensory cortex and into the surrounding higher order sensory cortices. In addition, secondary hotspots in the frontal cortex were evoked by whisker and visual stimulation, with the frontal hotspot for whisker deflection being more anterior and lateral compared to the frontal hotspot evoked by visual stimulation. Investigating axonal projections, we found that the somatosensory whisker cortex and the visual cortex directly innervated frontal cortex, with visual cortex axons innervating a region medial and posterior to the innervation from somatosensory cortex, consistent with the location of sensory responses in frontal cortex. In turn, the axonal outputs of these two frontal cortical areas innervate distinct regions of striatum, superior colliculus, and brainstem. Sensory input, therefore, appears to map onto modality-specific regions of frontal cortex, perhaps participating in distinct sensorimotor transformations, and directing distinct motor outputs. (C) The Authors. Published by SPIE under a Creative Commons Attribution 3.0 Unported License.

SPIE-Intl Soc Optical Eng2017

Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice

Rachel Aronoff, Carl Petersen

Tactile information is actively acquired and processed in the brain through concerted interactions between movement and sensation. Somatosensory input is often the result of self-generated movement during the active touch of objects, and conversely, sensory information is used to refine motor control. There must therefore be important interactions between sensory and motor pathways, which we chose to investigate in the mouse whisker sensorimotor system. Voltage-sensitive dye was applied to the neocortex of mice to directly image the membrane potential dynamics of sensorimotor cortex with subcolumnar spatial resolution and millisecond temporal precision. Single brief whisker deflections evoked highly distributed depolarizing cortical sensory responses, which began in the primary somatosensory barrel cortex and subsequently excited the whisker motor cortex. The spread of sensory information to motor cortex was dynamically regulated by behavior and correlated with the generation of sensory-evoked whisker movement. Sensory processing in motor cortex may therefore contribute significantly to active tactile sensory perception.

2007