Auditory map plasticity: diversity in causes and consequences

Abstract

Auditory cortical maps have been a long-standing focus of studies that assess the expression, mechanisms, and consequences of sensory plasticity. Here we discuss recent progress in understanding how auditory experience transforms spatially organized sound representations at higher levels of the central auditory pathways. New insights into the mechanisms underlying map changes have been achieved and more refined interpretations of various map plasticity effects and their consequences in terms of behavioral corollaries and learning as well as other cognitive aspects have been offered. The systematic organizational principles of cortical sound processing remain a key aspect in studying and interpreting the role of plasticity in hearing.

Figure 1

Mechanisms and unsolved mysteries underlying auditory cortical map reorganization. (a) Tonotopic best frequency (BF) map reconstructed from ~50 extracellular multiunit recording sites from the middle layers of mouse AI, each spaced ~100 μm apart (data from [18]) In addition to receiving heavy feedforward sensory input from the medial geniculate body, AI tonotopic organization is influenced by long-range neuromodulatory inputs such as dopaminergic (DA) inputs from the ventral tegmental area [141], noradrenergic (NA) inputs from locus coeruleus [142], serotinergic inputs from the dorsal raphe (5-HT) [143], glutamatergic inputs from the frontal cortex [144], and cholinergic (ACh) input from nucleus basalis [49]. Of these systems, retuning of auditory response properties by cholingeric modulation is by far the best understood. (b) Recent research has described a cortical microcircuit that translates associative learning cues from nucleus basalis into lasting reorganization of auditory response properties. During auditory fear learning, nociceptive inputs activate basalis afferents innervating layer I of auditory cortex, which excite layer I interneurons via nicotinic ACh receptors. These interneurons, in turn, inhibit parvalbumin+ interneurons in layer 2/3, thereby disinhibiting layer 2/3 pyramidal neurons and enabling plastic reorganization of sound-related excitatory inputs conveyed from layer IV neurons. However, basalis afferents also convey associative learning signals to deeper layers of the auditory cortex, where their effects are thought to be mediated by muscarinic ACh receptors. More work will be needed to reconstruct the organization of parallel microcircuits that translate basalis signals into plasticity of the deeper input/output layers of AI. (c) The synaptic basis for associative retuning of frequency selectivity has been characterized in experiments that isolate excitatory and inhibitory synaptic conductances onto AI neurons before and after a single tone frequency is repeatedly paired with electrical stimulation of nucleus basalis [117]. Before pairing, tone-evoked synaptic excitation and inhibition are precisely co-tuned for frequency. Within minutes of pairing, sound-evoked inhibition is selectively weakened at the paired frequency, followed by an intermediate unbalanced period when excitation has shifted to the paired frequency but inhibition is disorganized. Within an hour after pairing, synaptic excitation and inhibition have co-registered and remain tuned to the paired frequency for at least several hours before returning to their pre-pairing baseline tuning absent further bouts of associative learning cues from basalis. (d) Auditory maps can also be reorganized through non-associative plasticity mechanisms. For instance, within minutes following exposure to intense noise, spectral and temporal organization of sound-evoked inhibitory synaptic inputs are dysregulated, producing poorly selective ‘noisy’ receptive field organization [145]. Over the course of several weeks, AI neurons become re-tuned to sound frequencies bordering the cochlear lesion [64, 131] in a manner that may depend on homeostatic plasticity mechanisms [137] rather than associative plasticity mechanisms such as modulation from nucleus basalis [146]. (e) Additional work will be needed to unveil the specific homeostatic mechanisms that enable receptive field renormalization following auditory deafferentation. For instance, compensatory plasticity could be supported by scaling up postsynaptic responses to a reduced afferent signal, by changing the balance of synaptic excitation (E) and inhibition (I), or by altering the intrinsic electrical excitability of neurons through changing the levels or type of voltage-gated ion channels, as has been demonstrated in the auditory brainstem following changes in afferent activity levels [147, 148], but not in the cortex.