Associative learning and sensory neuroplasticity: how does it happen and what is it good for?

Abstract

Historically, the body's sensory systems have been presumed to provide the brain with raw information about the external environment, which the brain must interpret to select a behavioral response. Consequently, studies of the neurobiology of learning and memory have focused on circuitry that interfaces between sensory inputs and behavioral outputs, such as the amygdala and cerebellum. However, evidence is accumulating that some forms of learning can in fact drive stimulus-specific changes very early in sensory systems, including not only primary sensory cortices but also precortical structures and even the peripheral sensory organs themselves. This review synthesizes evidence across sensory modalities to report emerging themes, including the systems' flexibility to emphasize different aspects of a sensory stimulus depending on its predictive features and ability of different forms of learning to produce similar plasticity in sensory structures. Potential functions of this learning-induced neuroplasticity are discussed in relation to the challenges faced by sensory systems in changing environments, and evidence for absolute changes in sensory ability is considered. We also emphasize that this plasticity may serve important nonsensory functions, including balancing metabolic load, regulating attentional focus, and facilitating downstream neuroplasticity.

IGF1-Dependent Synaptic Plasticity of Mitral Cells in Olfactory Memory during Social Learning

“…However, memory formation is not completely abolished when the STFP-induced M-G-M synapse LTP is ablated by deletions of Syt10 or IGF1-R, suggesting that other synaptic modifications in other brain areas contribute to memory formation after STFP (Lesburgueres et al, 2011). Multiple types of synaptic plasticity distributed in different brain regions may coherently contribute to long-term memory formation (Lesburgueres et al, 2011; Takeuchi et al, 2014; McGann, 2015). …”

Persistent, generalized hypersensitivity of olfactory bulb interneurons after olfactory fear generalization

“…However, fear learning also induces dramatic changes in sensory regions (Bakin & Weinberger, 1990; Chen, Barnes, & Wilson, 2011; Fletcher, 2012; Gdalyahu, Tring, Polack, Gruver, Golshani, Fanselow et al, 2012; Li, Howard, Parrish, & Gottfried, 2008; McGann, 2015; Quirk, Armony, & LeDoux, 1997; Weinberger, 2007), including CS-specific hypersensitivity in primary sensory neurons (Dias & Ressler, 2014; Jones, Choi, Davis, & Ressler, 2008; Kass, Rosenthal, Pottackal, & McGann, 2013d). This plasticity can have explicitly sensory consequences, such as lowered detection thresholds (Ahs, Miller, Gordon, & Lundstrom, 2013; Parma, Ferraro, Miller, Ahs, & Lundstrom, 2015) or altered perceptual discrimination abilities (Aizenberg & Geffen, 2013; Chen et al, 2011; Fletcher & Wilson, 2002; Li et al, 2008; Resnik & Paz, 2015; Resnik et al, 2011), but it may also be important for non-sensory functions like recruiting attention or triggering defensive behavior (McGann, 2015). Fear generalization has been presumed to reflect changes in higher-order structures responding to sensory inputs (Ciocchi, Herry, Grenier, Wolff, Letzkus, Vlachos et al, 2010; Dunsmoor & Paz, 2015; Dunsmoor, Prince, Murty, Kragel, & LaBar, 2011a; Ghosh & Chattarji, 2015; Resnik & Paz, 2015), but sensory regions might be responsible for labeling CS-resembling stimuli as potentially threatening (Aizenberg & Geffen, 2013; Chen et al, 2011; Krusemark & Li, 2012; Miasnikov & Weinberger, 2012).…”

Conditioned inhibitory and excitatory gain modulations of visual cortex in fear conditioning: Effects of analysis strategies of magnetocortical responses

“…Animal and human neuroimaging studies should address this issue in the future. Irrespective of the origin of the modulatory control of visual cortex activity, we argue that conditioned excitatory and inhibitory visual cortex gain control assures maximal discriminability between threat-relevant and fearirrelevant cues according to current ideas about the function of neural plasticity changes in sensory cortex during learning (McGann, 2015).…”

“…These changes occur at very early processing stages within 50-90 ms after stimulus onset in visual (Keil, Stolarova, Moratti, & Ray, 2007;Steinberg, Brockelmann, Rehbein, Dobel, & Junghofer, 2013;Stolarova, Keil, & Moratti, 2006) and after 35 ms in auditory cortex (Quirk, Armony, & LeDoux, 1997). Recently, there has been increasing interest in the mechanisms underlying sensory gain control driven by associative learning (McGann, 2015). Therefore, current research has focused only on the excitatory component of increased neural processing of emotional stimuli; that is, how, for example, a fear-relevant positive conditioned stimulus (CS1) evokes greater activity in the early sensory cortex (Miskovic & Keil, 2012;Weinberger, 2015).…”