Learning enhances sensory processing in mouse V1 before improving behavior

Abstract

A fundamental property of visual cortex is to enhance the representation of those stimuli that are relevant for behavior, but it remains poorly understood how such enhanced representations arise during learning. Using classical conditioning in mice, we show that orientation discrimination is learned in a sequence of distinct behavioral stages, in which animals first rely on stimulus appearance before exploiting its orientation to guide behavior. After confirming that orientation discrimination under classical conditioning requires primary visual cortex (V1), we measured, during learning, response properties of V1 neurons. Learning improved neural discriminability, sharpened orientation tuning and led to higher contrast sensitivity. Remarkably, these learning-related improvements in the V1 representation were fully expressed before successful orientation discrimination was evident in the animals' behavior. We propose that V1 plays a key role early in discrimination learning to enhance behaviorally relevant sensory information.

Tracing the Trajectory of Sensory Plasticity across Different Stages of Speech Learning in Adulthood

“…Our results diverge from theories that suggest that perceptual learning is primarily driven by sensory processing enhancement [6, 7, 22], but closely align with the RHT which indicates low-level sensory enhancement emerges at expert stages of perceptual learning [9, 23, 24]. Consistent with RHT, we posit that novice performance is guided by abstract categorical representations [8, 9], likely the result of receptor-field plasticity at higher-levels of the sensory processing hierarchy [25].…”

“…Training can alter the low-level sensory encoding of newly acquired speech sound patterns [5]; however, the time-course, behavioral-relevance, and long-term retention of such sensory plasticity is unclear. Some theories argue that sensory plasticity underlying signal enhancement is immediate and critical to perceptual learning [6, 7]. Others, like the reverse hierarchy theory (RHT), posit a slower time-course for sensory plasticity [8].…”

NMDAR-dependent emergence of behavioral representation in primary visual cortex

“…For example, moment-to-moment changes in arousal level produce robust modulation of neuronal firing in V1 and alterations in perceptual ability [1][2][3][4] . Additionally, learning associations between sensory stimuli and behaviorally relevant outcomes can drive changes in neuronal structure, activity patterns, and perceptual ability [5][6][7][8][9][10][11][12][13][14] .…”

“…Most previous investigations of functional plasticity in V1 during learning have focused on modifications of sensory representations by neuronal activity. In both primates and rodents, repeated association between a visual stimulus and reward results in modification of feature selectivity (e.g., orientation preference) by single neurons [6][7][8][10][11][12][13][14][15] . Such representations are also strongly shaped by top-down influences reflecting levels of arousal or attention 3,4,16 , and prior stimulus expectation 17,18 .…”

Neural ensemble activity depends on stimulus type in mouse primary visual cortex

“…Stimuli and data acquisition. Our stimuli comprised a set of pseudorandomly presented sinusoidal drifting gratings at full contrast, 20 repetitions each, of 6 different SFs at 8 directions (1 s stimulus-ON time, with 1 s pre-stimulus time) at a constant 1.6 Hz temporal frequency, interleaved with 1 minute spontaneous activity after each full set at medium luminance (grey screen), which is common practice to estimate ongoing activity [40][41][42] . Throughout this manuscript, this stimulus type is termed mG, and its associated interleaved grey screen S1.…”