Triggering visually-guided behavior by holographic activation of pattern completion neurons in cortical ensembles

Abstract

15 Neuronal ensembles are building blocks of cortical activity yet it is unclear if they 16 have any causal role in behavior. Here we tested if the precise activation of 17 neuronal ensembles with two-photon holographic optogenetics in mouse primary 18 visual cortex alters behavioral performance in a visual task. Disruption of 19 behaviorally relevant cortical ensembles by activation of non-selective neurons 20 decreased behavioral performance whereas optogenetic targeting of as few as 21 two neurons with pattern completion capability from behaviorally relevant 22 ensembles improved task performance by reliably recalling the whole ensemble. 23 Moreover, in some cases, activation of two pattern completion neurons, in the 24 absence of visual stimulus, triggered correct behavioral responses. Our results 25 demonstrate a causal role of neuronal ensembles in a visually guided behavior 26 and suggest that ensembles could represent perceptual states. 27 28

Reduced Repertoire of Cortical Microstates and Neuronal Ensembles in Medically Induced Loss of Consciousness

“…To conclude, extending previous studies at the macroscale (Barttfeld et al, 2015;Hudetz et al, 2015;Lewis et al, 2012), our results provide evidence that during mLOC, functional connectivity of the cortex also breaks down at the microscale. Regarding general brain function, a number of mechanistic studies on local cortical circuit activity (Afraz et al, 2006;Carrillo-Reid et al, 2018;Houweling and Brecht, 2008;Huber et al, 2008;Salzman et al, 1990) have substantiated the hypothesis that local neural ensembles are functional building blocks of cognition (Hebb, 1949;Hopfield, 1982). Indeed, in a recent study, the precisely controlled simultaneous holographic activation of as few as two cortical neurons with pattern completion capabilities could trigger an entire local neural ensemble and alter performance in a visual task (Carrillo-Reid et al, 2018).…”

“…Regarding general brain function, a number of mechanistic studies on local cortical circuit activity (Afraz et al, 2006;Carrillo-Reid et al, 2018;Houweling and Brecht, 2008;Huber et al, 2008;Salzman et al, 1990) have substantiated the hypothesis that local neural ensembles are functional building blocks of cognition (Hebb, 1949;Hopfield, 1982). Indeed, in a recent study, the precisely controlled simultaneous holographic activation of as few as two cortical neurons with pattern completion capabilities could trigger an entire local neural ensemble and alter performance in a visual task (Carrillo-Reid et al, 2018). This implies that behavior, which is inherently based on the integration of information processed across cortical areas, can be altered by finescaled local neural activity.…”

High-performance microbial opsins for spatially and temporally precise perturbations of large neuronal networks

“…Microbial opsins, which flux ionic current in response to illumination, have empowered neuroscientists to causally perturb brain circuits, yielding fundamental insight into brain function (Fenno et al, 2011). Optogenetics with spatiotemporally patterned illumination enables investigators to causally relate precise features of neural activity with specific aspects of sensation, cognition, and action Marshel et al, 2019;Carrillo-Reid et al, 2019b;Gill et al, 2020;Daie et al, 2021;Anselmi et al, 2011;Dhawale et al, 2010;Lutz et al, 2008;Fan et al, 2020;Packer et al, 2012;Russell et al, 2021;Zhang et al, 2018;Packer et al, 2015;Rickgauer et al, 2014;Mardinly et al, 2018;Pe ´gard et al, 2017;Yang et al, 2018;Papagiakoumou et al, 2010;dal Maschio et al, 2017;Blumhagen et al, 2011;Farah et al, 2007;Fenno et al, 2011;Vaziri and Emiliani, 2012). However, the biophysical properties of the opsins employed, including their conductance, kinetics, and sensitivity, constrain the type and scale of perturbations that can be made (Cardin et al, 2009;Jun and Cardin, 2020;Hass and Glickfeld, 2016;Yu et al, 2020).…”

Brain computation by assemblies of neurons

“…This continues as long as x keeps firing, with certain cells in y t replaced by either "new winners" -cells that never participated in a y t with t < t -or by "old winners," cells that did participate in some y t with t < t. We say that the process has converged when when there are no new winners. Upon further firing of x, y t may evolve further slowly, or cycle periodically, with past winners coming in and out of y t ; in fact, this mode of assembly firing (cells of the assembly alternating in firing) is very much in accordance with how assemblies have been observed to fire in Ca+ imaging experiments in mice, see for example [6]. It is theoretically possible that a new winner cell may come up after convergence; but it can be proved that this is a highly unlikely event, and we have never noticed it in our simulations.…”

“…Pattern completion involves the firing, with some probability, of an assembly x following the firing of a few of its neurons [27,6]. Simulations in our model (Figure 1.F2) show that, indeed, if the creation of an assembly is completed with a sufficient number of activations of its parent, then by firing fewer than half of the neurons of the assembly will result in most, or essentially all, of the assembly firing.…”