Voltage-sensitive dye imaging reveals shifting spatiotemporal spread of whisker-induced activity in rat barrel cortex

Abstract

Lustig BR, Friedman RM, Winberry JE, Ebner FF, Roe AW. Voltage-sensitive dye imaging reveals shifting spatiotemporal spread of whiskerinduced activity in rat barrel cortex. J Neurophysiol 109: 2382-2392, 2013. First published February 6, 2013 doi:10.1152/jn.00430.2012.-In rats, navigating through an environment requires continuous information about objects near the head. Sensory information such as object location and surface texture are encoded by spike firing patterns of single neurons within rat barrel cortex. Although there are many studies using singleunit electrophysiology, much less is known regarding the spatiotemporal pattern of activity of populations of neurons in barrel cortex in response to whisker stimulation. To examine cortical response at the population level, we used voltage-sensitive dye (VSD) imaging to examine ensemble spatiotemporal dynamics of barrel cortex in response to stimulation of single or two adjacent whiskers in urethaneanesthetized rats. Single whisker stimulation produced a poststimulus fluorescence response peak within 12-16 ms in the barrel corresponding to the stimulated whisker (principal whisker). This fluorescence subsequently propagated throughout the barrel field, spreading anisotropically preferentially along a barrel row. After paired whisker stimulation, the VSD signal showed sublinear summation (less than the sum of 2 single whisker stimulations), consistent with previous electrophysiological and imaging studies. Surprisingly, we observed a spatial shift in the center of activation occurring over a 10-to 20-ms period with shift magnitudes of 1-2 barrels. This shift occurred predominantly in the posteromedial direction within the barrel field. Our data thus reveal previously unreported spatiotemporal patterns of barrel cortex activation. We suggest that this nontopographical shift is consistent with known functional and anatomic asymmetries in barrel cortex and that it may provide an important insight for understanding barrel field activation during whisking behavior. whisker function; optical imaging; somatosensory; barrel cortex; VSD IN RODENTS, THE TOPOGRAPHICAL single whisker-to-single cortical barrel relationship has long been recognized as a principle of cortical functional organization (Woolsey and Van der Loos 1970). Despite this clear one-to-one relationship, neurophysiological studies have revealed that principal whiskers are also modulated by subthreshold influences from distant sites (Brecht and

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.…”

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

“…30 for a review; also see Refs. [31][32][33][34][35][36][37][38]. Horizontal activity spreads may be important for integrating responses within and across sensory systems as well as for providing a substrate for associative learning and various other forms of adult plasticity.…”

All-optical mapping of barrel cortex circuits based on simultaneous voltage-sensitive dye imaging and channelrhodopsin-mediated photostimulation

“…In the case of the barrel cortex, measurements of single-neuron responses are of limited value when studying a circuit composed of many neurons of multiple cell types. 1 A more powerful approach comes by considering circuit function at the population level, while monitoring the contributions of individual neuron types. For example, it would be useful to activate specific neuronal subtypes in different columns or layers, while simultaneously recording the activity of populations of neurons from all regions.…”

“…The high spatial and temporal resolution of VSDs permits the tracking of circuit activity and establishing connectivity within and between all columns and layers of the barrel cortex, both in vivo [2][3][4] and in vivo as well. 1,[5][6][7] Over the past few decades, many types of VSDs have been synthesized, including dyes based on absorption or birefringence and fluorescence. 8,9 Among these, the fluorescence-based styryl dyes have been most successful for imaging activity in the mouse or rat brain.…”

“…All-optical mapping of barrel cortex circuits based on simultaneous voltage-sensitive dye imaging and channelrhodopsin-mediated photostimulation 1 …”