Spectrotemporal dynamics of auditory cortical synaptic receptive field plasticity

Abstract

The nervous system must dynamically represent sensory information in order for animals to perceive and operate within a complex, changing environment. Receptive field plasticity in the auditory cortex allows cortical networks to organize around salient features of the sensory environment during postnatal development, and then subsequently refine these representations depending on behavioral context later in life. Here we review the major features of auditory cortical receptive field plasticity in young and adult animals, focusing on modifications to frequency tuning of synaptic inputs. Alteration in the patterns of acoustic input, including sensory deprivation and tonal exposure, leads to rapid adjustments of excitatory and inhibitory strengths that collectively determine the suprathreshold tuning curves of cortical neurons. Long-term cortical plasticity also requires co-activation of subcortical neuromodulatory control nuclei such as the cholinergic nucleus basalis, particularly in adults. Regardless of developmental stage, regulation of inhibition seems to be a general mechanism by which changes in sensory experience and neuromodulatory state can remodel cortical receptive fields. We discuss recent findings suggesting that the microdynamics of synaptic receptive field plasticity unfold as a multi-phase set of distinct phenomena, initiated by disrupting the balance between excitation and inhibition, and eventually leading to wide-scale changes to many synapses throughout the cortex. These changes are coordinated to enhance the representations of newly-significant stimuli, possibly for improved signal processing and language learning in humans.

Comparative Aspects of Hearing in Vertebrates and Insects with Antennal Ears

“…This view accords with the finding that information within the insect brain is quickly distributed into multiple parallel (and decorrelated) streams for the separate extraction of individual stimulus features [77]. The vertebrate auditory system, in contrast, is a general-purpose and more flexible system that is shaped by learning [78][79][80][81], affected by mood [82], focused by attention [83][84][85], and one that influences and is influenced by other parts of the brain, both sensory [86] and motor [87] areas, to detect and interpret any sound that may be subjectively important at any particular moment. Our auditory system reconfigures its functional connectivity 'on the fly' [88,89].…”

Plasticity of Cortical Excitatory-Inhibitory Balance

“…In general, reorganization of cortical receptive fields or shifts in tuning curves involve increased responses to paired or overrepresented stimuli, in parallel with decreases in responses to the original best stimulus or a deprived stimulus (Feldman 2009, Hensch & Fagiolini 2005, Weinberger 2007). Increases in responses to sensory stimuli are now generally accepted to be due to LTP at paired or reinforced inputs (Buonomano & Merzenich 1998, Froemke & Martins 2011). Behaviorally, strengthening auditory thalamocortical inputs to the amygdala via BCM-type stimulation procedures is sufficient to enhance auditory fear conditioning in trained animals (Nabavi et al 2014).…”

Inhibitory and Excitatory Spike-Timing-Dependent Plasticity in the Auditory Cortex

“…In particular, adjustments of excitatory synaptic strength are believed to be a major mechanism by which cortical networks adapt to the statistics of sensory input, over a range of timescales from seconds to days (Buonomano and Merzenich, 1998; Froemke and Martins, 2011; Martin et al, 2000; McGaugh 2000). Earlier studies of synaptic plasticity in cortex and hippocampus examined how induction of long-term potentiation (LTP) and long-term depression (LTD) depended on the overall rate of electrical stimulation (Bienenstock et al, 1982; Bliss and Collingridge, 1993; Kirkwood et al, 1993; Malenka and Nicoll, 1999).…”