The influence of visual cortex on perception is modulated by behavioural state

Abstract

Correspondence to Michael Häusser: m.hausser@ucl.ac.uk Our understanding of the link between neural activity and perception remains incomplete. Microstimulation and optogenetic experiments have shown that manipulating cortical activity can influence sensory-guided behaviour or elicit artificial percepts. And yet, some perceptual tasks can still be solved when sensory cortex is silenced or removed, suggesting that cortical activity may not always be essential. Reconciling these findings, and providing a quantitative framework linking cortical activity and behaviour, requires knowledge of the identity of the cells being activated during the behaviour, the engagement of the local and downstream networks, and the cortical and behavioural state. Here, we performed two-photon population calcium imaging in L2/3 primary visual cortex (V1) of headfixed mice performing a visual detection task while simultaneously activating specific groups of neurons using targeted two-photon optogenetics during low contrast visual stimulation. Only activation of groups of cells with similar tuning to the relevant visual stimulus led to a measurable bias of detection behaviour. Targeted photostimulation revealed signatures of centre-surround, predominantly inhibitory and like-to-like connectivity motifs in the local network which shaped the visual stimulus representation and partially explained the change in stimulus detectability. Moreover, the behavioural effects depended on overall performance: when the task was challenging for the mouse, V1 activity was more closely linked to performance, and cortical stimulation boosted perception. In contrast, when the task was easy, V1 activity was less informative about performance and cortical stimulation suppressed stimulus detection.Altogether, we find that both the selective routing of information through functionally specific circuits, and the prevailing cortical state, make similarly large contributions to explaining the behavioural response to photostimulation. Our results thus help to reconcile contradictory findings about the involvement of primary sensory cortex in behavioural tasks, suggesting that the influence of cortical activity on behaviour is dynamically reassigned depending on the demands of the task.Understanding the relationship between cortical activity and perception remains one of the most fundamental

How many neurons are sufficient for perception of cortical activity?

“…The matched suppression that we observed in the local L2/3 network is in accordance with the general net inhibitory effect of pyramidal neuron stimulation observed in vivo (Chettih & Harvey, 2019;Mateo et al, 2011;Russell et al, 2019) and in detailed network models of cortex (Cai et al, 2020). This supports the idea that such networks operate in an inhibition-stabilized regime where one role of inhibition is to control strong recurrent excitation (Denève & Machens, 2016;Murphy & Miller, 2009;Ozeki et al, 2009;Pehlevan & Sompolinsky, 2014;Sanzeni et al, 2020;Tsodyks et al, 1997;van Vreeswijk & Sompolinsky, 1996;Wolf et al, 2014), though since our perturbations are not targeted to inhibitory neurons with specific tuning we cannot assess how functionally specific this architecture might be (Sadeh & Clopath, 2020).…”

Patterned perturbation of inhibition can reveal the dynamical structure of neural processing

“…Recent advances in optogenetic techniques are enabling us -at an unprecedented pace -to design perturbation protocols where a specific pattern (e.g. a specific sequence or spatiotemporal pattern of activity) is invoked in identified neurons (Emiliani et al, 2015;Ronzitti et al, 2017;Chernov et al, 2018;Zhang et al, 2018;Carrillo-Reid et al, 2019;Marshel et al, 2019;Russell et al, 2019;Tran, Prince and Richards, 2019). Our study here proposes that such technological advances are indeed necessary to reveal fundamental principles of cortical computation.…”

“…Several recent studies have in fact used such patterned perturbations to study cortical function with more precision, for example by recording neurons involved in specific tasks (e.g. natural visual processing or memory tasks) and reactivating them in order to instigate or suppress the relevant behavior (Chernov et al, 2018;Carrillo-Reid et al, 2019;Marshel et al, 2019;Russell et al, 2019;Tran, Prince and Richards, 2019). Optogenetic techniques have particularly been exploited to cast light on the regime of operation of cortical networks, especially regarding the role of feedforward versus recurrent pathways.…”

Memory consolidation and improvement by synaptic tagging and capture in recurrent neural networks

“…If the activity in the cell assembly following 8h-recall is higher, then there will be experimental evidence for memory improvement. Another promising approach to test memory improvement at the network level would be to use optogenetic stimulation in combination with activity measurements through calcium imaging, which is an established method being very suitable for in-vivo experiments [4,76], and can be tuned to deliver precise learning and recall stimulation [15,68].…”