Suppression of cortical representation through backward conditioning

Abstract

Temporal stimulus reinforcement sequences have been shown to determine the directions of synaptic plasticity and behavioral learning. Here, we examined whether they also control the direction of cortical reorganization. Pairing ventral tegmental area stimulation with a sound in a backward conditioning paradigm specifically reduced representations of the paired sound in the primary auditory cortex (AI). This temporal sequence-dependent bidirectional cortical plasticity modulated by dopamine release hypothetically serves to prevent the over-representation of frequently occurring stimuli resulting from their random pairing with unrelated rewards. C ortical stimulus feature representations can be reorganized by our experiences throughout life. In the auditory system, for example, frequency discrimination training results in a selective expansion of the cortical area representing the training frequencies (1). Simple auditory classical conditioning and instrumental conditioning can also modify the spectral receptive fields of cortical neurons, enhancing and suppressing responses evoked by the paired sound (2-9). Although response suppression effects have been puzzling, in general, these cortical plasticity effects are believed to underlie improved sensory discrimination, to enlarge and temporally organize the responding population, and to enhance the salience of conditioned stimuli (10-12).The activation of brain neuromodulator systems appears to be required for long-lasting plasticity in the adult cerebral cortex (7,(13)(14)(15)(16)(17)(18). Brain cholinergic and dopaminergic systems are activated in the cortex during learning (19)(20)(21)(22) and have been demonstrated to play important roles in cortical plasticity (7,15,(23)(24)(25)(26)(27)(28)(29). Cholinergic basal forebrain lesions or cortical cholinergic receptor blockade prevents cortical reorganization (13)(14)(15)(16)(17)(18). Systematically pairing the microstimulation of cholinergic basal forebrain or dopaminergic ventral tegmentum neurons with sensory stimulation induces distinctly different forms of cortical plasticity that parallel different aspects of change induced by behavioral training (1-4, 15, 23-28). The specific form of the cortical plasticity is likely determined by a number of factors, including the spectral, spatial, and temporal characteristics of the sensory input and the temporal sequence of the sensory and neuromodulator activation (15,(24)(25)(26).Studies of experience-dependent plasticity have demonstrated enhancement of cortical representations of behaviorally important stimuli, in which neuromodulators are involved presumably through a positive modulation of long-term potentiation (30-33), a putative cellular mechanism underlying plasticity (34, 35). Under certain circumstances, neuromodulators also enhance long-term depression (36, 37), suggesting that they may also mediate reduction of cortical representation.The temporal relationships of stimulus and reinforcement appear to be important for determining the directions of brain plast...

Intensive training in adults refines A1 representations degraded in an early postnatal critical period

“…However, these studies once again demonstrate that the adult auditory cortex remains plastic for attended, rewarded stimuli. It has been suggested that the interaction of auditory inputs, neuromodulator release, and top-down influences from higher auditory areas contribute to this learningbased cortical plasticity (20,(47)(48)(49)(50)(51)(52)(53)(54)(55). The fact that passive exposure to the same stimuli, when not reliably coupled to reward, has no measurable effect on frequency selectivity and tonotopicity of A1 in the present study again supports the conclusion that top-down modulation contributes significantly to learning-induced cortical plasticity in the adult brain (20).…”

Reward-timing-dependent bidirectional modulation of cortical microcircuits during optical single-neuron operant conditioning

“…Thus, our results indicate that the motor cortex can be a causal origin of the RTBM without signals from the prefrontal and parietal cortices, which are presumably required for cognitive strategies 5,10 . In the auditory cortex, forward conditioning of pure tone stimulation and electrical stimulation of dopaminergic ventral tegmental neurons increased the size of the cortical area responding to the tone frequency, and backward conditioning reduced the size of the area 30,31 . This bidirectional remodeling may share the same underlying mechanisms as RTBM in the motor cortex, although RTBM in the motor cortex was faster.…”

Sound sequence discrimination learning motivated by reward requires dopaminergic D2 receptor activation in the rat auditory cortex

“…Dopaminergic fibers have been found in the AC (Campbell et al 1987;Harper and Wallace 1995;Goldsmith and Joyce 1996). Neuronal plasticity in the AC is evoked by paired auditory and electrical stimulation of the ventral tegmental area (Bao et al 2001(Bao et al , 2003. Effects of D2 family antagonist on sound sequence discrimination learning.…”

“…Dopamine facilitates the induction of long-term potentiation (LTP) and long-term depression (LTD) in the neocortex (Law-Tho et al 1995;Otani et al 1998;Blond et al 2002). Neuronal plasticity in the AC is induced by sound stimulus paired with electrical stimulation in the ventral tegmental area (Bao et al 2001(Bao et al , 2003. In our previous behavioral study, water-deprived rats were trained to discriminate between sound sequences using a reward of water (Kudoh et al 2004).…”