Imaging spatiotemporal dynamics of surround inhibition in the barrels somatosensory cortex

“This activation can either lead to surround-activation or surround-inhibition of adjacent neurons (Derdikman et al., 2003), or may be coupled to other neuronal circuits involved in pain modulation or pain affect (Hofbauer et al.”

“…dyes (Shoham et al., 1999; Grinvald and Hildesheim, 2004) have allowed routine measurement of the spatiotemporal dynamics of sensory processing in head-fixed animals (Spors and Grinvald, 2002; Seidemann et al., 2002; Slovin et al., 2002; Petersen et al., 2003a, 2003b; Derdikman et al., 2003).”

“This timescale emerges whether assembly activation is measured in the sensory (Super et al., 2001; Slovin et al., 2002), somatosensory (Derdikman et al., 2003), or motor (Riehle et al., 1997) areas.”

“The ratio of excitation to inhibition decreases as a function of distance from the center, creating the “surround” inhibition (Simons and Carvell, 1989; Kleinfeld and Delaney, 1996; Takashima et al., 2001; Derdikman et al., 2003).”

“Waves in rodent barrel cortex, for instance, travel twice as fast along the rows than along the arcs (Derdikman et al., 2003; Petersen et al., 2003a), and this bias matches a bias in the axons of layer 2/3 pyramidal neurons, which extend preferentially along the rows (Petersen et al., 2003a).”

“In mammalian sensory cortex, sensory-evoked propagating waves were found in previous imaging studies using blue dyes (Derdikman et al., 2003; Petersen et al., 2003a; Roland et al., 2006).”

“Optical imaging of intrinsic signals and voltage-sensitive dyes average the responses over large populations of neurons [6,7,15–18].”

“…and may be associated with center-surround electrophysiological patterns of activity consisting of center excitation and surround inhibition (Cauli et al., 2004; Derdikman et al., 2003; Devor et al., 2007; Faraci and Breese, 1993; Faraci and Sobey, 1998; Hamel, 2006; Takashima et al., 2001).”

“Predominant inhibition is a common finding in the ipsilateral SI and the surround region in the contralateral SI (Derdikman et al., 2003; Devor et al., 2007).”

“(2003), Derdikman et al. (2003),”

“…et al. 1999; Contreras and Llinas 2001; Laaris and Keller 2002; Petersen and Sakmann 2001), and in vivo (Borgdorff et al. 2007; Civillico and Contreras 2006; Derdikman et al. 2003; Ferezou et al. 2006; Grinvald et al. 1984; Kleinfeld and Delaney 1996; Petersen et al. 2003a,b; Shoham et al. 1999).”

“Voltage sensitive dyes have been used to measure inhibition evoked by single whisker stimulation but the relative magnitudes of inhibition in surround compared with activated regions was not resolved (Derdikman et al., 2003).”

“…than in the center of the activated area, as evidenced both in the 3D map and in its cross section, resembling distributions observed previously in the CNS (von Békésy, 1967; Dudel, 1983; Contreras and Llinas, 2001; Derdikman et al., 2003; Petersen et al., 2003; Wirth and Lüscher, 2004).”

“There are many examples of inhibitory effect of nearby barrels on the whisker barrel of interest (Derdikman et al., 2003; Simons and Carvell, 1989).”

“In the rodent study, where rat barrel columns are on the order of 400 (Derdikman et al., 2003), we exclusively used400 μmstimulatingfibers to activate somatosensory cortex (and a spot size between 400 and 800 μm in diameter (Cayce et al.”

“cortical map boundaries in the normal brain (Zheng and Knudsen, 2001; Derdikman et al., 2003; Hensch and Stryker, 2004; Foeller et al., 2005).”

“Similar surround inhibition has been described during normal cortical processing (Derdikman et al., 2003; Devor et al., 2007) as well as during interictal spike activity (Schwartz and Bonhoeffer, 2001).”

“Common examples in which increased activity in one cortical region can cause an inhibitory surround include normal visual or somatosensory processing (Angelucci et al., 2002; Brumberg et al., 1996; Derdikman et al., 2003; McCasland et al., 1991; Sengpiel et al., 1997).”

“Cerebral Cortex April 2009;19:926--937 doi:10.1093/cercor/bhn141 Advance Access publication October 1, 2008”

“This comparison shows a great potential for in vivo imaging using the new blue dyes, as shown in recent reports (Derdikman et al. 2003; Ferezou et al. 2006; Grinvald and Hildesheim 2004; Petersen et al. 2003a,b; Shoham et al. 1999; Spors and Grinvald 2002).”

“, 2002), somatosensory (Derdikman et al., 2003) or motor areas (Riehle et al.”

“Apart from a few reports of successful imaging of inhibitory circuit activity through the use of voltage-sensitive dyes (Horikawa et al., 1996; Cohen and Yarom, 2000; Derdikman et al., 2003 ), autofluorescence (Ebner et al., 2005), pH indicators (Elias et al., 1993), and organic Cl � indicator dyes (Isomura et al., 20…”

“These whisker receptive fields are strongly shaped by PWand SW-evoked GABAergic inhibition (Brecht et al. 2003; Derdikman et al. 2003; Kyriazi et al. 1996a,b, 1998; Moore and Nelson 1998; Simons and Carvell 1989; Wilent and Contreras 2004).”

“In the barrel cortex, voltage-sensitive dye recordings in vivo revealed how sensory stimulation activates a spatial pattern of surround and rebound inhibition followed by 16-Hz oscillations (Derdikman et al. 2003).”

“Modular networks in closed-loop systems realized to interface the DAQ MATERIALS AND METHODS The setup developed for experiments of embodied electrophysiology is characterized by several different software, hardware and wetware components ( Figure1 ).”

“Accumulated evidence using multiple techniques (intracellular and extracellular recordings; optical imaging based on voltage-sensitive dyes, optical imaging based on intrinsic signals, evoked potential mapping) have demonstrated large, frequently symmetric, areas of activation within barrel cortex after single whisker…”

“2 Seconds [26], comparable to numerous observations in-vivo [1,27–29].”

“DOI: 10.7554/eLife.16420 17 of 24 in multiple studies (Brecht and Sakmann, 2002; Derdikman et al., 2003; Civillico and Contreras, 2006; Ollerenshaw et al., 2012a).”

“It is also the time required to activate a single cortical column (Derdikman et al., 2003).”

“Single whisker stimulation evokes depolarization that begins in the corresponding barrel, spreads across the entire extent of barrel cortex and then into adjacent cortical areas (Kleinfeld and Delaney, 1996; Derdikman et al., 2003; Petersen et al., 2003; Ferezou et al., 2006, 2007; Frostig et al., 2008; Davis et al.,…”

“…unit studies and imaging studies using voltage-sensitive dyes likewise have shown that excitation in the responding neuronal population is accompanied by the development of a surrounding field of inhibition (Brumberg et al. 1996; Derdikman et al. 2003; Foeller et al. 2005; Wirth and Luscher 2004).”

“…using single unit (Hubel and Wiesel, 1968; Woolsey and Van der Loos, 1970) and population recordings (Orbach et al., 1985; Bonhoeffer and Grinvald, 1991; Kleinfeld and Delaney, 1996; Derdikman et al., 2003) that neurons with similar functional properties and receptive fields are clustered in space.”

“As self-sustained entities, they propagate or move about in space [4–8 , 10– Propagating coherent patterns have been registered in the experimental literature as ‘‘spreading’’ or ‘‘drifting’’ activity [4–8] or as ‘‘traveling waves’’ [13–24].”

“5), contrary to Derdikman et al. (2003).”

“…dyes, autofluorescence, pH indicators, and organic Cl- indicator dyes (Elias et al., 1993; Horikawa et al., 1996; Cohen and Yarom, 2000; Derdikman et al., 2003; Isomura et al., 2003; Ebner et al., 2005), analysis of neural circuits has been limited by the lack of effective techniques…”

“Derdikman et al. (2003) reported a hyperpolarizing response following a depolarizing response to whisker deflection and attributed this observation to the use of the blue dye RH1692.”

“It was expected from previously published results that multiple response components would be observable in both the SEP and imaging datasets: four components in SEP data [composed of two positive and two negative waveforms (Di & Barth, 1991)] and two components in imaging data [one positive and one negative (Derdikman…”

“(2007) showed that the NBR around a stimulated location is associated with arteriovascular constriction and a decrease in membrane potential (a hyperpolarization) in the surround (Derdikman et al., 2003; Devor et al., 2005).”

“…somatosensory cortex and their full functional interpretation should assume the presence of spatial and temporal inhibition (Laskin and Spencer, 1979; Simons, 1985; Brumberg et al., 1996; Xing and Gerstein, 1996; DiCarlo and Johnson, 2002; Derdikman et al., 2003; Wirth and Luscher, 2004).”

“Stimuli consisted of brief 150-ms puffs of air delivered to the vibrissa array on one side of the face (Ahissar et al. 2000; Derdikman et al. 2003; Sosnik et al. 2001).”

“In the cortex of naïve mice, this was evident by the anatomical confinement of astrocytic processes to the barrel borders at layer IV, in which the well-defined neuronal columns are linked to functional properties (Derdikman et al., 2003; Woolsey et al., 1996).”

“[27, 17]) are of particular interest in neuroscience, and particles and gliders bear more than a passing resemblance to these coherent structures.”

“Extensive electrophysiological and imaging analyses in vivo suggest that brain modularity is a key determinant of our cognitive capacities, having impacts on both dynamic and functional aspects of neural activity (Hubel &Wiesel, 1977; Sporns et al., 2000; Derdikman et al., 2003; Diamond et al., 2003; Op de Beeck et al…”

“Many studies, especially of sensory cortices, have investigated information processing within and between these sub-regions of the cortex (Dehnardt et al., 1999; Derdikman et al., 2003; Haidarliu and Ahissar, 2001; Petersen and Sakmann, 2001).”

“It can be assumed that just layer 2/3 pyramids are involved in spatiotemporal integration of sensory activity, including the regulatory momentum of recurrent inhibition (Derdikman et al. 2003).”

“[23] are presumably implemented by long-range excitation of local inhibitory neurons [32], as is thought to be the case in V1 for high contrast visual inputs (see refs.”

“Deep layers V and VI have specific function in thalamocorticothalamic loops and thus for auditory stimulus conveyed through the thalamus (de Ribaupierre et al., 1972; Steriade, 1999; Derdikman et al., 2003; Castro-Alamancos, 2004).”

“, 1979) and invasive imaging of rat cortex (Derdikman et al. 2003), it is believed that a larger area of cortex is activated during the P35m than during the N20m, which is consistent with the increased amplitude of the response that we see in our data.”

“Neurons in the surround region are hyperpolarized, which has been attributed to inhibition, but firing is unaffected (Kleinfeld and Delaney 1996; Derdikman et al. 2003; Devor et al. 2007).”

“Such multicolumn models may provide insights into the mechanisms of more complex cortico-cortical interactions such as surround [63,64] and transcallosal inhibition in SI [65–67].”

“Stimulation of surrounding whiskers up to inter-stimulus intervals of 30 ms suppresses the input from the principal whisker (Simons 1983; Derdikman et al. 2003).”

“The deflection of a single whisker initially evokes a highly localized sensory response, mapping onto the appropriate barrel column in the primary somatosensory cortex (S1).(3,5,11) However, the sensory response typically spreads over the next milliseconds, invading neighboring cortical barrel columns, depending upon…”

“In the somatosensory barrel cortex, suppression of the neuronal activity in surround barrels may be involved in contrast enhancement of principal whisker signaling (Brumberg et al. 1996; Derdikman et al. 2003; Sachdev et al. 2012).”

“tactile stimulation of the skin), the balance 539 between local excitation and inhibition reveal a network of opposing activated and suppressed 540 domains[71,72].”

“In the barrel field of mice and rats this happened 16–36 ms after the start of stimulation of single whiskers (Derdikman et al., 2003; Petersen et al., 2003a; Civillico and Contreras, 2006, 2012; Ferezou et al., 2006, 2007; Lippert et al., 2007).”

“Recent studies employing voltage-sensitive dye (vsd) imaging in vivo have shown this technique to be well suited for visualizing the spread of activity between cortical columns (Kleinfeld and Delaney 1996; Derdikman et al. 2003; Petersen et al. 2003).”

“The voltage-sensitive dye RH1691 [11,14] was dissolved at 2 mg/ml in buffer solution containing (in mM): 126 NaCl, 3.”

“For example, examining astrocyte remodeling during development (Diamond et al., 1993; Olavarria et al., 1987), or studying the impact of functional deprivation, such as removing a single or a row of vibrissae on astrocyte morphology.”

“Erchova et al., 2002) as well as intracellular and calcium imaging data (Moore and Nelson, 1998; Higley and Contreras, 2003; Derdikman et al., 2003 ).”

“When the tip of a whisker was gently moved, optical signals were observed in the corresponding cortical barrel field (Derdikman et al. 2003).”

“Moreover, the dominant neuronal response time of sensory cortices peaks with similar constants across regions and species 30,35,36 , suggesting a conserved temporal motif in cortical computation.”

“Such waves have been described in the primary visual [2], [3] and somatosensory cortices of mammals [ 4 ]–[6], including humans [7].”

“…1994; Bringuier et al., 1999; Contreras and Llinás, 2001), somatosensory cortex (Kleinfeld and Delaney, 1996; Ghanzafar and Nicoleilis, 1999; Contreras and Llinás, 2001; Petersen et al., 2003; Derdikman et al., 2003), frontal cortex (Seidemann et al., 2002) and hippocampus (Traub et al., 1991).”