Precise Spatiotemporal Patterns among Visual Cortical Areas and Their Relation to Visual Stimulus Processing

“Proposed mechanisms, such as binding by synchrony (Singer and Gray, 1995) or enhanced neural response (Roelfsema, 2006), follow the Gestalt laws of similarity and good continuation and are consistent with known patterns of horizontal cortical connections (Stettler et al.”

“A plausible interpretation of this observation is that topdown patterns are imprints of the high-level knowledge required to perform perceptual grouping and correctly segment natural images (Hupé et al., 1998; Lamme and Roelfsema, 2000; Bullier et al., 2001).”

“We extracted PEs from the VSDI signal and showed that these PEs correlate with increased spiking activity and negative LFP peaks previously shown to be synchronized with action potentials from local neuronal populations (Beggs and Plenz, 2003).”

“Indeed, recently it was shown that reduced activity in early visual areas, possibly due to cortical feedback from higher visual areas, is involved in the facilitation of object recognition (Murray et al., 2002; Bar et al., 2006; Summerfield et al., 2006).”

“To detect microsaccades that occurred during the trials, we employed the algorithm proposed by Engbert and Kliegl (2003).”

“Another model that may account for the type of patterns reported in this work is the synfire chain model (Abeles, 1982a,b; Abeles, 1991), which predicts the propagation of synchronous activity within neuronal groups (“pools”) with high temporal precision.”

“…high-level cues (Palmer, 1992) and are supported by a rich network of feedforward, horizontal, and feedback connections (Rockland and Lund, 1982; Gilbert and Wiesel, 1989; Malach et al., 1993; Salin and Bullier, 1995; Hupé et al., 1998, 2001; Galuske et al., 2002; Stettler et al., 2002;…”

“Engel et al. (1991b) demonstrated that synchronous neuronal oscillations may serve to establish relationships between stimulus features processed in different areas of visual cortex.”

“A plausible interpretation of this observation is that topdown patterns are imprints of the high-level knowledge required to perform perceptual grouping and correctly segment natural images (Hupé et al., 1998; Lamme and Roelfsema, 2000; Bullier et al., 2001).”

“Numerous studies have reported the existence of such patterns in various cortical areas (Dayhoff and Gerstein, 1983; Abeles et al., 1993; Prut et al., 1998; Lestienne et al., 1999; Ikegaya et al., 2004; Shmiel et al., 2005).”

“These values are well within the published range (Van Essen et al., 1984; Angelucci et al., 2002; Chen et al., 2006).”

“Their proposed role in visual processing is consistent with, but also extends, the mechanism of binding by synchrony (Engel et al., 1991a,b; Engel et al., 1992; Gray et al., 1992; Eckhorn, 1994; Burgess and O’Keefe, 1996; Huxter et al., 2003).”

“…regime to repeated epochs of spontaneous synaptic potentials or ‘‘motifs”; these were detected in cortical slices and in vivo (Mao et al., 2001; Cossart et al., 2003; Ikegaya et al., 2004; MacLean et al., 2005), but it was later claimed that they could also arise by chance from the mere…”

“Suggested mechanisms of perceptual grouping and segmentation use both low-level and high-level cues (Palmer, 1992) and are supported by a rich network of feedforward, horizontal, and feedback connections (Rockland and Lund, 1982; Gilbert and Wiesel, 1989; Malach et al., 1993; Salin and Bullier, 1995; Hupé et al., 1998…”

“…free, fixation only); hence, to remove this noise we calculated the average blank signal (i.e., average over all blank trials within an imaging session, typically, n 30) and subtracted it from each stimulus-evoked trial pixelwise (Grinvald et al., 1994; Arieli et al., 1995; Shoham et al., 1999).”

“Since the dye we used responds to membrane depolarization by an increase in fluorescence (Grinvald and Hildesheim, 2004), this point process effectively extracts epochs of simultaneously increased activation (i.e., depolarization) in local population activity (see Figs.”

“Suggested mechanisms of perceptual grouping and segmentation use both low-level and high-level cues (Palmer, 1992) and are supported by a rich network of feedforward, horizontal, and feedback connections (Rockland and Lund, 1982; Gilbert and Wiesel, 1989; Malach et al., 1993; Salin and Bullier, 1995; Hupé et al., 1998…”

“Their proposed role in visual processing is consistent with, but also extends, the mechanism of binding by synchrony (Engel et al., 1991a,b; Engel et al., 1992; Gray et al., 1992; Eckhorn, 1994; Burgess and O’Keefe, 1996; Huxter et al., 2003).”

“They are also consistent with cross-correlation analysis of single units in the visual cortex as well as with known anatomical connectivity of visual areas (Gilbert et al., 1996; Smith and Kohn, 2008).”

“…horizontal spread of activity mediated by long-range, nonmyelinated connections, whereas the faster conduction values could be the result of propagation by myelinated axons either in feedforward pathways or feedback from higher cortical areas (Grinvald et al., 1994; Bringuier et al., 1999).”

“…and are supported by a rich network of feedforward, horizontal, and feedback connections (Rockland and Lund, 1982; Gilbert and Wiesel, 1989; Malach et al., 1993; Salin and Bullier, 1995; Hupé et al., 1998, 2001; Galuske et al., 2002; Stettler et al., 2002; Bullier, 2004; Shmuel et al., 2005).”

“Indeed, recently it was shown that reduced activity in early visual areas, possibly due to cortical feedback from higher visual areas, is involved in the facilitation of object recognition (Murray et al., 2002; Bar et al., 2006; Summerfield et al., 2006).”

“Although the binding-by-synchrony model posits that the presence of dynamic synchrony or spatiotemporal patterns during visual processing should correlate positively with perceptual grouping (Kreiter and Singer, 1996), other models might actually predict a negative correlation.”

“The second late phase was previously reported to be associated with higher visual functions such as pop out, grouping, and figure–ground segregation (Supèr et al., 2001).”

“Engel et al. (1991b) demonstrated that synchronous neuronal oscillations may serve to establish relationships between stimulus features processed in different areas of visual cortex.”

“Proposed mechanisms, such as binding by synchrony (Singer and Gray, 1995) or enhanced neural response (Roelfsema, 2006), follow the Gestalt laws of similarity and good continuation and are consistent with known patterns of horizontal cortical connections (Stettler et al.”

“In addition, it has been shown that the VSDI signal in each pixel sums the activity of membrane potentials from a few hundred neurons (Grinvald et al., 1999; Petersen et al., 2003).”

“…synaptic potentials or ‘‘motifs”; these were detected in cortical slices and in vivo (Mao et al., 2001; Cossart et al., 2003; Ikegaya et al., 2004; MacLean et al., 2005), but it was later claimed that they could also arise by chance from the mere stochastic properties of cortical activity…”

“For example, it has been shown that response latency is contrast dependent and varies by tens of milliseconds (Gawne et al., 1996).”

“…use both low-level and high-level cues (Palmer, 1992) and are supported by a rich network of feedforward, horizontal, and feedback connections (Rockland and Lund, 1982; Gilbert and Wiesel, 1989; Malach et al., 1993; Salin and Bullier, 1995; Hupé et al., 1998, 2001; Galuske et al., 2002;…”

“, average over all blank trials within an imaging session, typically, n 30) and subtracted it from each stimulus-evoked trial pixelwise (Grinvald et al., 1994; Arieli et al., 1995; Shoham et al., 1999).”

“They are also consistent with cross-correlation analysis of single units in the visual cortex as well as with known anatomical connectivity of visual areas (Gilbert et al., 1996; Smith and Kohn, 2008).”

“…beyond the spiking regime to repeated epochs of spontaneous synaptic potentials or ‘‘motifs”; these were detected in cortical slices and in vivo (Mao et al., 2001; Cossart et al., 2003; Ikegaya et al., 2004; MacLean et al., 2005), but it was later claimed that they could also arise by chance…”

“…and are supported by a rich network of feedforward, horizontal, and feedback connections (Rockland and Lund, 1982; Gilbert and Wiesel, 1989; Malach et al., 1993; Salin and Bullier, 1995; Hupé et al., 1998, 2001; Galuske et al., 2002; Stettler et al., 2002; Bullier, 2004; Shmuel et al., 2005).”

“Their proposed role in visual processing is consistent with, but also extends, the mechanism of binding by synchrony (Engel et al., 1991a,b; Engel et al., 1992; Gray et al., 1992; Eckhorn, 1994; Burgess and O’Keefe, 1996; Huxter et al., 2003).”

“Suggested mechanisms of perceptual grouping and segmentation use both low-level and high-level cues (Palmer, 1992) and are supported by a rich network of feedforward, horizontal, and feedback connections (Rockland and Lund, 1982; Gilbert and Wiesel, 1989; Malach et al.”

“Numerous studies have reported the existence of such patterns in various cortical areas (Dayhoff and Gerstein, 1983; Abeles et al., 1993; Prut et al., 1998; Lestienne et al., 1999; Ikegaya et al., 2004; Shmiel et al., 2005).”

“It has been suggested that these patterns can serve as a mechanism to temporally bind spatially distributed cortical activity that generate a coherent visual object, cognitive function, or motor action (von der Malsburg, 1985; Bienenstock, 1995).”

“…studies, however, have demonstrated that in natural images, opportunities for spurious local grouping are so pervasive that segmentation based solely on local features is often ineffective; high-level knowledge must then be brought to bear on decisions underlying grouping (Ullman, 1995).”

“It has been argued that repeats of spatiotemporal patterns may occur by chance (Oram et al., 1999; Baker and Lemon, 2000), calling into question the existence of reliable mechanisms exploiting such patterns (Richmond et al., 1999).”

“To correct for the nonhomogeneous illumination pattern and because the optical response is proportional to the illumination level, the recorded values at each pixel were divided by the average value at that pixel before stimulus onset i.e., background-fluorescence (Slovin et al., 2002).”

“The protocol of data acquisition in VSDI has been described in detail elsewhere (Shtoyerman et al., 2000).”

“It has been suggested that these patterns can serve as a mechanism to temporally bind spatially distributed cortical activity that generate a coherent visual object, cognitive function, or motor action (von der Malsburg, 1985; Bienenstock, 1995).”

“A plausible interpretation of this observation is that topdown patterns are imprints of the high-level knowledge required to perform perceptual grouping and correctly segment natural images (Hupé et al., 1998; Lamme and Roelfsema, 2000; Bullier et al., 2001).”

“These values are well within the published range (Van Essen et al., 1984; Angelucci et al., 2002; Chen et al., 2006).”

“The surgical procedure has been reported in detail elsewhere (Grinvald et al., 1999; Shtoyerman et al., 2000; Arieli et al., 2002).”

“It has been argued that repeats of spatiotemporal patterns may occur by chance (Oram et al., 1999; Baker and Lemon, 2000), calling into question the existence of reliable mechanisms exploiting such patterns (Richmond et al., 1999).”

“Their proposed role in visual processing is consistent with, but also extends, the mechanism of binding by synchrony (Engel et al., 1991a,b; Engel et al., 1992; Gray et al., 1992; Eckhorn, 1994; Burgess and O’Keefe, 1996; Huxter et al., 2003).”

“nization of different synfire chains, which has been proposed as a substrate for hierarchical composition (Bienenstock, 1996; Abeles et al., 2004; Hayon et al., 2005), i.”

“Suggested mechanisms of perceptual grouping and segmentation use both low-level and high-level cues (Palmer, 1992) and are supported by a rich network of feedforward, horizontal, and feedback connections (Rockland and Lund, 1982; Gilbert and Wiesel, 1989; Malach et al., 1993; Salin and Bullier, 1995; Hupé et al., 1998…”

“Suggested mechanisms of perceptual grouping and segmentation use both low-level and high-level cues (Palmer, 1992) and are supported by a rich network of feedforward, horizontal, and feedback connections (Rockland and Lund, 1982; Gilbert and Wiesel, 1989; Malach et al., 1993; Salin and Bullier, 1995; Hupé et al., 1998…”

“Numerous studies have reported the existence of such patterns in various cortical areas (Dayhoff and Gerstein, 1983; Abeles et al., 1993; Prut et al., 1998; Lestienne et al., 1999; Ikegaya et al., 2004; Shmiel et al., 2005).”

“The first was phase perturbation (Rainer et al., 2001), which generated images with 10% phase coherence.”

“, 2005), but it was later claimed that they could also arise by chance from the mere stochastic properties of cortical activity (Mokeichev et al., 2007).”

“The number of significantly repeating patterns reported here is much higher than those published previously (Prut et al., 1998; Ikegaya et al., 2004; Shmiel et al., 2006).”

“These findings have been considered an indication of functional connectivity or formation of task-dependent assemblies of cooperative neurons (Dayhoff and Gerstein, 1983; Lestienne and Strehler, 1987; Prut et al., 1998).”

“The statistical significance of the counts of pattern occurrences (doublets or triplets) was assessed by comparing their occurrence in real raster plots with their occurrence in surrogate raster plots generated by two independent methods (Hatsopoulos et al., 2003).”

“Numerous studies have reported the existence of such patterns in various cortical areas (Dayhoff and Gerstein, 1983; Abeles et al., 1993; Prut et al., 1998; Lestienne et al., 1999; Ikegaya et al., 2004; Shmiel et al., 2005).”

“…of different synfire chains, which has been proposed as a substrate for hierarchical composition (Bienenstock, 1996; Abeles et al., 2004; Hayon et al., 2005), i.e., vertical binding, would give rise to a subset of patterns that would depend on the computations carried out in the…”

“Indeed, the flow of information between areas was previously shown to be affected by the spatial complexity of a stimulus (Salazar et al., 2004).”

“It has been argued that repeats of spatiotemporal patterns may occur by chance (Oram et al., 1999; Baker and Lemon, 2000), calling into question the existence of reliable mechanisms exploiting such patterns (Richmond et al., 1999).”

“Numerous studies have reported the existence of such patterns in various cortical areas (Dayhoff and Gerstein, 1983; Abeles et al., 1993; Prut et al., 1998; Lestienne et al., 1999; Ikegaya et al., 2004; Shmiel et al., 2005).”

“To identify sequential pairs of neurons with fixed time intervals, we performed an exhaustive matching algorithm that searches for a given time interval in all of the possible combinations of active neurons (Ayzenshtat et al., 2010).”

“VSD recordings under similar experimental conditions do not show these high-frequency oscillations (Slovin et al., 2002; Chen et al., 2006; Meirovithz et al., 2010; Ayzenshtat et al., 2010), probably because of the low-pass filtering inherent in the VSD signal (Wu et al.”

“Interactions both within and between columns in visual cortex have demonstrated dynamic spatiotemporal patterns which are thought to represent the binding of features for cortical processing (Engel et al., 1990; Singer and Gray, 1995; von der Malsburg, 1995; Buzsaki and Draguhn, 2004; Fries, 2009; Ayzenshtat et al., 2…”

“…evoked by visual stimuli have been performed using VSD in rats (Xu et al., 2007; Han et al., 2008), ferrets (Roland et al., 2006; Harvey et al., 2009), cats (Jancke et al., 2004; Benucci et al., 2007; Sharon et al., 2007), and monkeys (Sit et al., 2009; Ayzenshtat et al., 2010), but never in mice.”

“In the work of Ayzenshtat et al. (2010) and Tal and Abeles (2016) the authors defined and extracted special events from their analog recordings (voltage-sensitive dye imaging and MEG, respectively) and reduced them to point events.”

“The in vivo VSD signal is highly correlated with the membrane potential, emphasizing subthreshold fluctuation (Sterkin et al., 1998; Petersen et al., 2003) but also reflecting spiking activity (Jancke et al., 2004; Ayzenshtat et al., 2010; Reynaud et al., 2011; Chen et al., 2012).”

“6 ) and scrambled versions of these images (Ayzenshtat et al. 2010) or an image of randomly oriented and positioned Gabor matrices (11 3 8 ).”

“…(1) defining region-of-interest (ROI; only pixels with fluorescence level 15% of maximal fluorescence were analyzed), (2) normalizing to background fluorescence, (3) average blank subtraction (see schematic illustration of the basic VSDI analysis by Ayzenshtat et al., 2010, their supplemental Fig.”

“…et al., 2006; Ferezou et al., 2007; Lippert et al., 2007; Xu et al., 2007; Ahmed et al., 2008; Han et al., 2008; Takagaki et al., 2008; Yoshida et al., 2008; Harvey et al., 2009; Ayzenshtat et al., 2010; Meirovithz et al., 2010; Ng et al., 2010; Polack and Contreras, 2012; Harvey and Roland, 2013).”

“For example, it has been shown that precise chains of activity can determine visual input (Ayzenshtat et al., 2010) in monkeys and predict their reaching (Abeles et al., 1993), opening a puzzle box (Prut et al., 1998), moving a joystick (Hatsopoulos et al., 2003), and drawing (Shmiel et al., 2006).”

“To do so, we first rank ordered the pixels according to the mutual information (MI) between the neuronal signal and the stimulus category in the set of training trials (Ayzenshtat et al., 2010).”

“…avoids biased sampling of neurons, captures population activity irrespective of receptive field locations, and preferred feature selectivities (Jancke et al. 1999; Jancke 2000), thus faithfully providing the global state of the cortex under different stimulus conditions (Ayzenshtat et al. 2010).”

“More recently, Ayzenshtat et al. (2010) described spatio-temporal patterns within and across early visual areas that contained enough information to reliably discriminate between stimulus categories.”

“ness or low spatial resolution [26–28].”

“[61] Supplementary Fig.”

“This notion might also be supported by reports that neural activity patterns can vary depending on the context of sensory stimuli, or on motor activity such as eye movement 24–30 .”

“However, we cannot exclude that feedback signals originating from higher visual areas with larger receptive field sizes than in primary visual cortex could add to these interactions 56,57 .”

“Our results, as well as many previous publications from the groups of Petersen, Slovin and Seidemann (Chen et al., 2006, 2008, 2012; Ferezou et al., 2006, 2007; Sit et al., 2009; Meirovithz et al., 2009, 2012; Ayzenshtat et al., 2010; Palmer et al., 2012; Chen et al., 2011; Chen and Seidemann, 2012), indicate that und…”

“The basic analysis of the VSDI signal is detailed previously (Slovin et al., 2002; Ayzenshtat et al., 2010, their supplemental Fig.”

“Such motion of (net excitatory) synaptic activity is also observed in other species and other visual stimulus conditions (Eriksson and Roland, 2006; Roland et al., 2006; Xu et al., 2007; Ahmed et al., 2008; Takagaki et al., 2008; Harvey et al., 2009; Roland, 2010; Ayzenshtat et al., 2010).”

“…patterns are known to be an essential element in visual processing, the spatiotemporal components (STCs) are also very important (Ahlfors et al., 1999; Ayzenshtat et al., 2010; Ioannides et al., 2012; van de Nieuwenhuijzen et al., 2013) and might be beneficial for the decoding of visual processing.”

“Spiking responses to omitted stimuli can reflect an unexpected change or reconstruction of the specific omitted image.”

“The Rho GTPase family kinases (signalization network downstream of NMDAR and AMPAR) communicate with the calcium-dependent kinase CAMKII and are able to spread laterally tens of microns away from the original LTP site [67–69].”

“Our stimulus-driven task induced a specific spatial pattern of beta (16–25 Hz) activation similar to the stimulus-specific activation map imaged with voltage-sensitive dyes in monkey primary cortex [48].”

“…Senseman, 1996; Roland, 2002; Slovin et al., 2002; Petersen et al., 2003; Jancke et al., 2004; Ferezou et al., 2006; Roland et al., 2006; Ahmed et al., 2008; Eriksson et al., 2008; Harvey et al., 2009; Ayzenshtat et al., 2010; Chavane et al., 2011; Harvey and Roland, 2013; Müller et al., 2014).”

“Spatio-temporal activity patterns play an important role in cortical mechanisms of information processing (Ayzenshtat et al., 2010).”

“Local cortical network dynamic and spatio-temporal cortical dynamics Local networks in the cortex interact spatially to contribute to cortical functions (Arieli et al. 1995; Ferezou et al. 2007; Ayzenshtat et al. 2010; Iacaruso et al. 2017; Roland et al. 2017; Davis et al. 2020; Grün et al. 2022).”

“large neural populations of a brain of a living animal with high spatio-temporal resolution [1,2,3].”

“There are already approaches available to image with parallel cell recordings from the acute brain slices (Tominaga et al. 2001; Carlson and Coulter 2008; Ayzenshtat et al. 2010; Mapelli et al. 2010; Ferrea et al. 2012).”

“Whereas a considerable amount of experimental in vivo data was acquired over the years through combined intracellular (sharp or whole-cell) and LFP recordings, in both anesthetized and awake animals, so far only a few studies combined imaging and LFP recording (e.g., Ferezou et al. 2007; Ayzenshtat et al. 2010) (see e…”

“32,34 Briefly, to remove the background fluorescence levels, each pixel was normalized to its baseline fluorescence level (average over few frames before stimulation onset).”

“…activity was observed repeatedly in VSD imaging of the visual cortex in the awake, behaving monkey (Chen et al., 2006; Meirovithz et al., 2010; Ayzenshtat et al., 2010), and it became a generally accepted view that large-amplitude, sensory-evoked propagating waves were predominantly an…”

“In experimental neurosciences the recording techniques are multiple: intracellular and extracellular recordings (ER), electroencephalography, functional magnetic resonance imaging (fMRI), two-photons imaging, voltage sensitive dye optical imaging (VSDi), etc.”