Selective Activation of a Putative Reinforcement Signal Conditions Cued Interval Timing in Primary Visual Cortex

Abstract

Summary As a consequence of conditioning visual cues with delayed reward, cue-evoked neural activity that predicts the time of expected future reward emerges in the primary visual cortex (V1). We hypothesized that this reward timing activity is engendered by a reinforcement signal conveying reward acquisition to V1. In lieu of behavioral conditioning, we assessed in vivo whether selective activation of either basal forebrain (BF) or cholinergic innervation is sufficient to condition cued interval timing activity. Substituting for actual reward, optogenetic activation of BF or cholinergic input within V1 at fixed delays following visual stimulation entrains neural responses that mimic behaviorally-conditioned reward timing activity. Optogenetically-conditioned neural responses express cue-evoked temporal intervals that correspond to the conditioning intervals, are bidirectionally modifiable, display experience-dependent refinement, and exhibit a scale invariance to the encoded delay. Our results demonstrate that the activation of BF or cholinergic input within V1is sufficient to encode cued interval timing activity, and indicate that V1 itself is a substrate for associative learning that may inform the timing of visually-cued behaviors.

Theta Oscillations in Visual Cortex Emerge with Experience to Convey Expected Reward Time and Experienced Reward Rate

“…Computational studies have shown that cue-reward intervals can be expressed in V1 single units through reward-dependent expression of synaptic plasticity (Gavornik et al, 2009;Gavornik and Shouval, 2011). According to this reward-dependent expression model, V1 receives a local reinforcement signal, as recently experimentally observed (Liu et al, 2015), that selectively enables changes in synaptic weights of those synapses that have been active in the recent past. The population reward timing signal evidenced in V1's LFP arises with training as a result of oscillations becoming longer or shorter to match the animal's behavioral reward time.…”

“…Cortical representations of visual inputs in the adult animal can be modified by a variety of manipulations, such as repeated exposure (Fiorentini and Berardi, 1980;Furmanski et al, 2004;Frenkel et al, 2006;Gavornik andBear, 2014), visual deprivation (Sawtell et al, 2003;Hofer et al, 2006), attentional demands (Ahissar and Hochstein, 1993;Fahle, 2004), and positive reinforcements (Serences, 2008;Seitz et al, 2009;Stȃnişor et al, 2013). These changes in V1 responses are generally interpreted in a perceptual learning framework, wherein visual experience improves our ability to perceive the world (Karmarkar and Dan, 2006;Gilbert et al, 2009;Roelfsema et al, 2010). Here we demonstrate that, with training, stimulus-evoked oscillations in V1 lose their relationship with the physical parameters of the stimuli and evolve to relate to the behavioral meaning, as acquired through training, that the stimuli foretell: reward time and prior reward history but not reward magnitude itself.…”

“…Furthermore, theta oscillations are associated with induction of synaptic plasticity (Buzsáki, 2002). Within the visual system, oscillatory activity has been implicated in selective attention (Fries et al, 2001;Palva and Palva, 2007;Schroeder and Lakatos, 2009), working memory (Jensen, 2002;Lee et al, 2005), and interregional communication (Gray et al, 1989; Singer and Gray, 1995; Liebe et al, 2012) among other processes. If the visually evoked oscillations described here are related to these pro-cesses, one might expect to have observed either a facilitatory or deleterious effect on the animal's behavior; yet we did not observe any differences in animal's performance in trials with, versus without, oscillations.…”

Vision: How to Train Visual Cortex to Predict Reward Time

“…But which part of your brain is actually involved in generating this expectation? In a series of recent papers [1][2][3], one published in this issue of Current Biology [4], Shuler and colleagues present a surprising answer: it is, at least in part, your primary visual cortex.…”

“…These reward-timing responses come in three different varieties: some neurons show sustained activation from stimulus presentation to the expected time of reward, others show inhibition during the same period, and a third group exhibits a firing rate peak at the expected reward time ( Figure 1B). Liu et al [4] in this issue build on this work to better understand the mechanisms by which V1 neurons can be trained to exhibit such responses.…”