This study aimed to identify neural mechanisms that underlie perceptual learning in a visual-discrimination task. We trained two monkeys (Macaca mulatta) to determine the direction of visual motion while we recorded from their middle temporal area (MT), which in trained monkeys represents motion information that is used to solve the task, and lateral intraparietal area (LIP), which represents the transformation of motion information into a saccadic choice. During training, improved behavioral sensitivity to weak motion signals was accompanied by changes in motion-driven responses of neurons in LIP, but not in MT. The time course and magnitude of the changes in LIP correlated with the changes in behavioral sensitivity throughout training. Thus, for this task, perceptual learning does not appear to involve improvements in how sensory information is represented in the brain, but rather how the sensory representation is interpreted to form the decision that guides behavior.

We recently showed that improved perceptual performance on a visual motion direction-discrimination task corresponds to changes not in how sensory information is represented in the brain but rather how that information is interpreted to form a decision that guides behaviour. Here we show that these changes can be accounted for using a reinforcement learning rule to shape functional connectivity between the sensory and decision neurons. We modelled performance based on the readout of simulated responses of direction-selective sensory neurons in the middle temporal area (MT) of monkey cortex. A reward prediction error guided changes in connections between these sensory neurons and the decision process, first establishing the association between motion direction and response direction and then gradually improving perceptual sensitivity by selectively strengthening the connections from the most sensitive neurons in the sensory population. The results suggest a common, feedback-driven mechanism for some forms of associative and perceptual learning.

Gold JI, Law C-T, Connolly P, Bennur S. The relative influences of priors and sensory evidence on an oculomotor decision variable during perceptual learning. J Neurophysiol 100: 2653-2668. First published August 27, 2008 doi:10.1152/jn.90629.2008. Choice behavior on simple sensory-motor tasks can exhibit trial-to-trial dependencies. For perceptual tasks, these dependencies reflect the influence of prior trials on choices that are also guided by sensory evidence, which is often independent across trials. Here we show that the relative influences of prior trials and sensory evidence on choice behavior can be shaped by training, such that prior influences are strongest when perceptual sensitivity to the relevant sensory evidence is weakest and then decline steadily as sensitivity improves. We trained monkeys to decide the direction of random-dot motion and indicate their decision with an eye movement. We characterized sequential dependencies by relating current choices to weighted averages of prior choices. We then modeled behavior as a drift-diffusion process, in which the weighted average of prior choices provided an additive offset to a decision variable that integrated incoming motion evidence to govern choice. The average magnitude of offset within individual training sessions declined steadily as the quality of the integrated motion evidence increased over many months of training. The trial-by-trial magnitude of offset was correlated with signals related to developing commands that generate the oculomotor response but not with neural activity in either the middle temporal area, which represents information about the motion stimulus, or the lateral intraparietal area, which represents the sensory-motor conversion. The results suggest that training can shape the relative contributions of expectations based on prior trends and incoming sensory evidence to select and prepare visually guided actions. I N T R O D U C T I O NPerformance on trial-based sensory-motor tasks can exhibit numerous forms of sequential dependence. For example, both response times and choice are sensitive to effects of the previous trial, including repeated actions, task switching, and errors (Botvinick et al. 2001;Cho et al. 2002;Laming 1979Laming 1968Luce 1986). For tasks in which reward probability depends on sequential patterns of choices, these dependencies can reflect rational strategies for choosing future outcomes based on prior history Behrens et al. 2007;Corrado et al. 2005;Davidson and McCarthy 1988;Herrnstein 1961;Kennerley et al. 2006;Lau and Glimcher 2005;Sugrue et al. 2004;Williams 1988). In contrast, for perceptual tasks in which the present stimulus is the exclusive factor determining the rewarded choice, these dependencies can only hinder performance. The goal of this study was to better understand how these dependencies evolve as perceptual sensitivity to sensory cues that instruct the rewarded choice improves with training.We trained monkeys on a one-interval, two-alternative direction-discrimination task in which they d...

Recent findings in humans and animals suggest that sleep promotes synaptic plasticity, but the underlying mechanisms have not been identified. We have demonstrated recently an important role for sleep in ocular dominance (OD) plasticity, a classic form of in vivo cortical remodeling triggered by monocular deprivation (MD) during a critical period of development. The mechanisms responsible for the effects of sleep on OD plasticity are unknown but may depend on neuronal activity in the sleeping brain. We investigated the role of cortical activity in sleep-dependent plasticity by reversibly inactivating the sleeping visual cortex (V1) after a period of MD. Critical period cats were bilaterally implanted with cannulas in V1 and standard EEG/EMG electrodes for polysomnographic recording. After a period of MD, visual cortices were infused with the sodium channel blocker lidocaine in vehicle or vehicle only during sleep. A third group of cats served as sham controls and were infused with lidocaine outside of V1 (into the CSF). Both optical imaging of intrinsic cortical signals and microelectrode recordings showed that OD plasticity was significantly reduced in cats whose visual cortices were reversibly silenced during sleep. These findings demonstrate that the mechanisms governing this form of sleep-dependent plasticity require cortical activity. They provide an important insight into how sleep modifies synaptic circuitry by narrowing the range of possible candidate mechanisms to those that are activity dependent.

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