Theta oscillations in visual cortex emerge with experience to convey expected reward time and experienced reward rate

The primary visual cortex (V1) is widely regarded as faithfully conveying the physical properties of visual stimuli. Thus, experience-induced changes in V1 are often interpreted as improving visual perception (i.e., perceptual learning). Here we describe how, with experience, cue-evoked oscillations emerge in V1 to convey expected reward time as well as to relate experienced reward rate. We show, in chronic multisite local field potential recordings from rat V1, that repeated presentation of visual cues induces the emergence of visually evoked oscillatory activity. Early in training, the visually evoked oscillations relate to the physical parameters of the stimuli. However, with training, the oscillations evolve to relate the time in which those stimuli foretell expected reward. Moreover, the oscillation prevalence reflects the reward rate recently experienced by the animal. Thus, training induces experience-dependent changes in V1 activity that relate to what those stimuli have come to signify behaviorally: when to expect future reward and at what rate.Fil: Zold, Camila Lidia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay; Argentina. Universidad de Buenos Aires. Facultad de Medicina; ArgentinaFil: Hussain Shuler, Marshall G.. University Johns Hopkins; Estados Unido

The hunt for the perfect discounting function and a reckoning of time perception

Making decisions that factor the cost of time is fundamental to survival. Yet, while it is readily appreciated that our perception of time is intimately involved in this process, theories regarding intertemporal decision-making and theories regarding time perception are treated, largely, independently. Even within these respective domains, models providing good fits to data fail to provide insight as to why, from a normative sense, those fits should take their apparent form. Conversely, normative models that proffer a rationalization for why an agent should weigh options in a particular way, or to perceive time in a particular way, fail to account for the full body of well-established experimental evidence. Here we review select, yet key advances in our understanding, identifying conceptual breakthroughs in the fields of intertemporal decision-making and in time perception, as well as their limits and failings in the face of hard-won experimental observation. On this background of accrued knowledge, a new conception unifying the domains of decision-making and time perception is put forward (Training-Integrated Maximization of Reinforcement Rate, TIMERR) to provide a better fit to observations and a more parsimonious reckoning of why we make choices, and thereby perceive time, the way we do

A general theory of intertemporal decision-making and the perception of time

Animals and humans make decisions based on their expected outcomes. Since relevant outcomes are often delayed, perceiving delays and choosing between earlier versus later rewards (intertemporal decision-making) is an essential component of animal behavior. The myriad observations made in experiments studying intertemporal decision-making and time perception have not yet been rationalized within a single theory. Here we present a theory-Training--Integrated Maximized Estimation of Reinforcement Rate (TIMERR)--that explains a wide variety of behavioral observations made in intertemporal decision-making and the perception of time. Our theory postulates that animals make intertemporal choices to optimize expected reward rates over a limited temporal window; this window includes a past integration interval (over which experienced reward rate is estimated) and the expected delay to future reward. Using this theory, we derive a mathematical expression for the subjective representation of time. A unique contribution of our work is in finding that the past integration interval directly determines the steepness of temporal discounting and the nonlinearity of time perception. In so doing, our theory provides a single framework to understand both intertemporal decision-making and time perception.Comment: 37 pages, 4 main figures, 3 supplementary figure

The Timing of Reward-Seeking Action Tracks Visually-Cued Theta Oscillations in Primary Visual Cortex

An emerging body of work challenges the view that primary visual cortex (V1) represents the visual world faithfully. Theta oscillations in the local field potential (LFP) of V1 have been found to convey temporal expectations and, specifically, to express the delay between a visual stimulus and the reward that it portends. We extend this work by showing how these oscillatory states in male, wild-type rats can even relate to the timing of a visually cued reward-seeking behavior. In particular, we show that, with training, high precision and accuracy in behavioral timing tracks the power of these oscillations and the time of action execution covaries with their duration. These LFP oscillations are also intimately related to spiking responses at the single-unit level, which themselves carry predictive timing information. Together, these observations extend our understanding of the role of cortical oscillations in timing generally and the role of V1 in the timing of visually cued behaviors specifically.Fil: Levy, Joshua M.. University Johns Hopkins; Estados UnidosFil: Zold, Camila Lidia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Fisiología y Biofísica Bernardo Houssay. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Fisiología y Biofísica Bernardo Houssay; ArgentinaFil: Namboodiri, Vijay Mohan K.. University of North Carolina; Estados UnidosFil: Hussain Shuler, Marshall G. University Johns Hopkins; Estados Unido

What does scalar timing tell us about neural dynamics?

The “Scalar Timing Law,” which is a temporal domain generalization of the well known Weber Law, states that the errors estimating temporal intervals scale linearly with the durations of the intervals. Linear scaling has been studied extensively in human and animal models and holds over several orders of magnitude, though to date there is no agreed upon explanation for its physiological basis. Starting from the assumption that behavioral variability stems from neural variability, this work shows how to derive firing rate functions that are consistent with scalar timing. We show that firing rate functions with a log-power form, and a set of parameters that depend on spike count statistics, can account for scalar timing. Our derivation depends on a linear approximation, but we use simulations to validate the theory and show that log-power firing rate functions result in scalar timing over a large range of times and parameters. Simulation results match the predictions of our model, though our initial formulation results in a slight bias toward overestimation that can be corrected using a simple iterative approach to learn a decision threshold.R01MH093665K99MH09965

Cannabinoid Receptor Blockade Reveals Parallel Plasticity Mechanisms in Different Layers of Mouse Visual Cortex

SummaryThe ocular dominance (OD) shift that occurs in visual cortex after brief monocular deprivation (MD) is a classic model of experience-dependent cortical plasticity. It has been suggested that OD plasticity in layer 2/3 of visual cortex precedes and is necessary for plasticity in the thalamocortical input layer 4. Here, we show in mouse visual cortex that rapid OD plasticity occurs simultaneously in layers 2/3 and 4. Remarkably, pharmacological blockade of cannabinoid receptors completely prevents the OD shift in layer 2/3, leaving plasticity intact in layer 4. Thus, experience-dependent cortical modifications in layers 2/3 and 4 can occur in parallel, via distinct mechanisms. These findings simplify the mechanistic description of plasticity in layer 4, force a revision in the interpretation of previous studies in which laminar differences in OD plasticity mechanisms were unrecognized, and have important implications for the therapeutic use of cannabinoid receptor antagonists in humans

A Cholinergic Mechanism for Reward Timing within Primary Visual Cortex

Neurons in rodent primary visual cortex (V1) relate operantly conditioned stimulus-reward intervals with modulated patterns of spiking output, but little is known about the locus or mechanism of this plasticity. Here we show that cholinergic basal forebrain projections to V1 are necessary for the neural acquisition, but not the expression, of reward timing in the visual cortex of awake, behaving animals. We then mimic reward timing in vitro by pairing white matter stimulation with muscarinic receptor activation at a fixed interval and show that this protocol results in the prolongation of electrically evoked spike train durations out to the conditioned interval. Together, these data suggest that V1 possesses the circuitry and plasticity to support reward time prediction learning and the cholinergic system serves as an important reinforcement signal which, in vivo, conveys to the cortex the outcome of behavior.National Eye Institute (Grant R01 EYO12309)Eunice Kennedy Shriver National Institute of Child Health and Human Development (U.S.) (Grant R01 HD046943

Optogenetic Dissection of the Basal Forebrain Neuromodulatory Control of Cortical Activation, Plasticity, and Cognition

The basal forebrain (BF) houses major ascending projections to the entire neocortex that have long been implicated in arousal, learning, and attention. The disruption of the BF has been linked with major neurological disorders, such as coma and Alzheimer's disease, as well as in normal cognitive aging. Although it is best known for its cholinergic neurons, the BF is in fact an anatomically and neurochemically complex structure. Recent studies using transgenic mouse lines to target specific BF cell types have led to a renaissance in the study of the BF and are beginning to yield new insights about cell-type-specific circuit mechanisms during behavior. These approaches enable us to determine the behavioral conditions under which cholinergic and noncholinergic BF neurons are activated and how they control cortical processing to influence behavior. Here we discuss recent advances that have expanded our knowledge about this poorly understood brain region and laid the foundation for future cell-type-specific manipulations to modulate arousal, attention, and cortical plasticity in neurological disorders