Stimulus relevance modulates contrast adaptation in visual cortex

Abstract

A general principle of sensory processing is that neurons adapt to sustained stimuli by reducing their response over time. Most of our knowledge on adaptation in single cells is based on experiments in anesthetized animals. How responses adapt in awake animals, when stimuli may be behaviorally relevant or not, remains unclear. Here we show that contrast adaptation in mouse primary visual cortex depends on the behavioral relevance of the stimulus. Cells that adapted to contrast under anesthesia maintained or even increased their activity in awake naïve mice. When engaged in a visually guided task, contrast adaptation re-occurred for stimuli that were irrelevant for solving the task. However, contrast adaptation was reversed when stimuli acquired behavioral relevance. Regulation of cortical adaptation by task demand may allow dynamic control of sensory-evoked signal flow in the neocortex.DOI: http://dx.doi.org/10.7554/eLife.21589.001

Opposing forms of adaptation in mouse visual cortex are controlled by distinct inhibitory microcircuits and gated by locomotion

“…Similarly, how do the effects of locomotion compare with other changes in behavioural or cognitive state, such as those associated with spatial attention or conditioning to a reward stimulus? A recent study indicates that sensitization becomes the dominant form of adaptation when a mouse is conditioned to a rewarded stimulus (Keller et al, 2017). The results we have presented may provide a framework for understanding the circuit mechanisms underlying this effect and perhaps other changes in internal state that alter the processing of stimuli originating from the external world.…”

“…Neurons expressing the calcium reporter GCaMP6f were imaged in Layer 2/3 and stimuli consisted of drifting sinusoidal gratings presented for 10 s (20º visual field, 80% contrast, 1 Hz, see Methods). The duration of the stimulus was chosen based on the similar time-scale of adaptive effects observed in the retina (Ozuysal and Baccus, 2012;Johnston et al, 2019) and, more recently, in V1 of awake mice (Keller et al, 2017). The responsivity of neurons in V1 is strongly dependent on locomotion (Niell and Stryker, 2010;Fu et al, 2014) so we began by confining our analysis to measurements made while the mouse was running on a trackball.…”

“…Adaptation to contrast as a depressing response has been observed throughout the visual system, beginning in the synaptic output of retinal bipolar cells (Ozuysal and Baccus, 2012;Nikolaev et al, 2013), through retinal ganglion cells (Smirnakis et al, 1997), the dorsal lateral geniculate nucleus (dLGN) (Solomon et al, 2004;King et al, 2016) and V1 (Benucci et al, 2013;Bonin et al, 2006;Dhruv and Carandini, 2014;King et al, 2016;Wilson et al, 2012). But adaptation in V1 is not simply inherited from the retina: local processing generates time-dependent changes in gain of PCs, although the circuit mechanisms remain unclear (Dhruv and Carandini, 2014;King et al, 2016;Keller et al, 2017).…”

“…Cholinergic inputs from the basal forebrain activated during running excite VIP interneurons which results in excitation of PCs through a VIP->SST disinhibition pathway (Fu et al, 2014;Niell and Stryker, 2010;Pakan et al, 2016;Dipoppa et al, 2018). We have less understanding of the role of inhibitory circuits in controlling adaptation to a visual stimulus (Harris and Shepherd, 2015;King et al, 2016), in part because most physiological studies of sensory cortex have used anaesthetized animals in which inhibitory mechanisms are defective, altering fundamental aspects of circuit function including adaptation (Haider et al, 2013;Keller et al, 2017).…”

Learning differentially reorganizes brain activity and connectivity

“…It is interesting to speculate that changes in activity provide support for the early steep increases in performance, and changes in connectivity provide support for the later fine-tuning of behavior when performance gains from trial to trial are relatively small [35][36][37] . The early role of activity in explaining performance could in part be due to the fact that early stimulus encoding produces activity patterns that represent the objects being learned, and the accuracy and differentiation between those representations is critical for accurate responses in the task 38,39 .…”