Whisker array functional representation in rat barrel cortex: transcendence of one-to-one topography and its underlying mechanism

Abstract

The one-to-one relationship between whiskers, barrels, and barrel columns described for rat barrel cortex demonstrates that the organization of cortical function adheres to topographical and columnar principles. Supporting evidence is typically based on a single or few whiskers being stimulated, although behaving rats rely on the use of all their whiskers. Less is known about the cortical response when many whiskers are stimulated. Here, we use intrinsic signal optical imaging and supra- and sub-threshold electrophysiology recordings to map and characterize the cortical response to an array of all large whiskers. The cortical response was found to possess a single peak located centrally within a large activation spread, thereby no longer conveying information about the individual identities of the stimulated whiskers (e.g., many local peaks). Using modeling and pharmacological manipulations, we determined that this single central peak, plus other salient properties, can be predicted by and depends on large cortical activation spreads evoked by individual whisker stimulation. Compared to single whisker stimulation, the peak magnitude was comparable in strength and the response area was 2.6-fold larger, with both exhibiting a reduction in variability that was particularly pronounced (3.8x) for the peak magnitude. Findings extended to a different collection (subset) of whiskers. Our results indicate the rat barrel cortex response to multi-site stimulation transcends one-to-one topography to culminate in a large activation spread with a single central peak, and offer a potential neurobiological mechanism for the psychophysical phenomenon of multi-site stimulation being perceived as though a single, central site has been stimulated.

Neuronal networks and mediators of cortical neurovascular coupling responses in normal and altered brain states

“…Glutamate released by thalamocortical afferents targets multiple cortical cells expressing glutamatergic receptors, such as pyramidal cells, GABA interneurons and astrocytes, and triggers the increases in intracellular calcium (Ca 2þ ) required for the release of vasoactive messengers [30]. In summary, the barrel cortex contains a topographical representation of each whisker, allowing precise assessment of the relationship between evoked neuronal activity, the underlying neuronal network [43,44], and changes in CBF induced by stimulation of any given whisker or group of whiskers [45].…”

Photonics meets connectomics: case of diffuse, long-range horizontal projections in rat cortex

“…1). 24,26,27 Depending on the whisker stimulated, the activity can extend past the barrel field of somatosensory cortex and can cross cytoarchitectonic borders into visual cortex (VCx), auditory cortex, or the trunk representation in somatosensory cortex ( Fig. 1).…”

“…24,26 We have detected the horizontal spread of activity electrophysiologically as a change in local field potential as well as by intrinsic signal optical imaging. 24,27 Evidence for similar long-range horizontal spreads of activity evoked by single whisker stimulation can be gleaned from numerous other studies involving both rats and mice and employing a wide variety of recording techniques, although many of these other studies emphasize different aspects of the activity pattern (see Ref. 30 for a review; also see Refs.…”

“…The combined activity of multiple such axons might then explain the spread of subthreshold activity that we have observed. 24,27 Using this strategy, we have reconstructed dozens of axons extending horizontally for long distances from various rAAV injection sites distributed across the neocortex. Numerous long, border-crossing horizontal axons also have been reconstructed from brains injected with an rAAV vector employing a calciumcalmodulin dependent protein kinase II alpha (CaMKIIα) promoter.…”

Review of mesoscopic optical tomography for depth-resolved imaging of hemodynamic changes and neural activities

“…[87][88][89] The barrel fields are close to the brain surface, therefore, many imaging studies have been carried out at this region. 10,[90][91][92][93][94][95][96][97][98] However, virtually all of the previous in vivo VSD cortical imaging studies obtain only 2-D depth-integrated responses, lacking depth-dependent information. Recently, by combining aFLOT with VSDs, in vivo 3-D neural activities in the whisker barrel cortex of mice following deflection of a single whisker have been demonstrated with 5-ms temporal resolution.…”