Set and setting: How behavioral state regulates sensory function and plasticity

Highlights

• Effects of three behavioral state features (attention, reinforcement, and vigilance) are described in specific sensory systems.

• Attention decreases discrimination thresholds for attended stimuli, and increases thresholds for non-attended stimuli.

• Various reinforcement parameters and reward cues can be encoded at the level of primary sensory cortices.

• Changes in neuromodulation and network activity during sleep are associated with plasticity in sensory systems.

Abstract

Recently developed neuroimaging and electrophysiological techniques are allowing us to answer fundamental questions about how behavioral states regulate our perception of the external environment. Studies using these techniques have yielded surprising insights into how sensory processing is affected at the earliest stages by attention and motivation, and how new sensory information received during wakefulness (e.g., during learning) continues to affect sensory brain circuits (leading to plastic changes) during subsequent sleep. This review aims to describe how brain states affect sensory response properties among neurons in primary and secondary sensory cortices, and how this relates to psychophysical detection thresholds and performance on sensory discrimination tasks. This is not intended to serve as a comprehensive overview of all brain states, or all sensory systems, but instead as an illustrative description of how three specific state variables (attention, motivation, and vigilance [i.e., sleep vs. wakefulness]) affect sensory systems in which they have been best studied.

Introduction

What determines the brain’s state?

“The universe is an intelligence test”.

– Timothy Leary (Wilson, 1977).

In 1964, psychologist Timothy Leary described sensory experience (in this case, channeled through the lens of psychedelic drug use) as a function of “set and setting” (Leary, Metzner, & Alpert, 1995). The term “set” refers to the internal state of the individual; “setting” refers to external stimuli. The question of how neurons and neural circuits respond to sensory stimuli has received extensive study. A relatively unexplored question is how one’s “set”, or internal state, determines how these neurons and circuits process sensory information. Ultimately, how we experience the outside world can be seen as a function of both sensory input (our setting) and the state of our internal sensory processing systems (our set).

How is an organism’s “set” set? The term “state” can refer to motivation, emotion, attention, consciousness, or arousal. All of these brain states can be altered by either external context (e.g., in the case of attention, by distracting stimuli) or internal factors (e.g., fatigue, hormones, and neuromodulator levels). Certain internal factors are (relatively speaking) immutable: one obvious example is genetics (Bendesky and Bargmann, 2011, Plomin and Craig, 1997). Other internal factors can be modulated in a dynamic way over the lifespan, through behavioral, environmental, and pharmacological manipulations. This review is focused on describing neural mechanisms that affect sensory function during states of attention, motivation, and vigilance (sleep and wakefulness). These states affect both how incoming sensory information is received (i.e., how neurons respond to sensory input), and how neuronal responses are altered over time by changing sensory input (i.e., sensory plasticity).